Big brained bats
Yes, it's the expensive bat testicle hypothesis:
The analysis of 334 species of bat found that in species where the females were promiscuous, the males had evolved larger testes but had relatively small brains. In species, where the females were monogamous, the situation was reversed. Male fidelity appeared to have no influence over testes or brain size.
Both brain tissue and sperm cells require a lot of metabolic energy to produce and maintain. The different species appear to have evolved a preference for developing one organ more than the other, presumably determined by which will help them produce more offspring.
This makes perfect sense to me, but the researchers were surprised:
Pitnick and his colleagues had predicted that, in species with promiscuous females, males would require bigger brains in order avoid being cuckolded. So they were surprised to find the opposite: "Perhaps monogamy is more neurologically demanding."
I guess it depends what they use them for. I wonder if there is some other factor correlated with both monogamy and brain size, for example -- like body size, or diet. This isn't the first time that bats have figured into the expensive tissue story, after all --- there is this paper by Jones and MacLarnon (2004) that shows that fruit-eating bats have larger brains than non-fruit-eaters, and that brain mass significantly covaries with gestation length. I suppose if monogamous species have longer gestations, that might explain that relation.
Drowning statistics
I got curious about drowning as a global cause of death tonight, so I did some research and found a paper by Etienne Krug et al. (2000).
The traditional view of injuries as "accidents," or random events, has resulted in the historical neglect of this area of public health. However, the most recent estimates show that injuries are among the leading causes of death and disability in the world. They affect all populations, regardless of age, sex, income, or geographic region. In 1998, about 5.8 million people (97.9 per 100 000 population) died of injuries worldwide, and injuries caused 16% of the global burden of disease (Krug et al. 2000:523).
The statistics on low- and middle-income countries are the most relevant. Drowning caused 22.4 deaths per 100 000 among children 0-4 years, making it the eleventh leading cause of death in that age group. The top ten were mostly infectious diseases (pneumonia, diarrheal disease, measles and malaria being the biggest), except for perinatal conditions and malnutrition.
The real importance of drowning was in the 5-14 year age class, where it was the fourth leading cause of death, accounting for 14.5 deaths per 100 000. That puts it ahead of diarrhal diseases for that age class, and more important than HIV, war, tuberculosis, and violence combined.
Drowning remains important for adults 15-44, as the ninth leading cause of death accounting for 5.7 per 100 000. It is a larger cause of death than maternal hemorrhage (although that applies only to women, naturally). In contrast, it was not in the top fifteen for older adults.
It is sort of unusual as a cause of death that has substantial importance for some of the lowest-mortality age classes. And it strikes me that it would be a substantial risk for a "coastal" adaptation -- exposing children to the water today (remembering that many aren't anywhere near water!) creates a global risk comparable to malaria.
References:
Krug EG, Sharma GK, Lozano R. 2000. The global burden of injuries. Am J Public Health 90:523-526. PubMed
Gorillapause
I missed this story back in December about menopause in captive gorillas:
Many biologists believe menopause evolved because it gave human grandmothers more time to help care for their grandchildren, said Steve Austad, a researcher at the University of Texas Health Science Center in San Antonio who was not involved in the study.
The new findings argue against the so-called "grandmother hypothesis," because female gorillas in the wild migrate away from their family groups and don't hang around to care for the grandkids.
Instead of an evolutionary adaptation, menopause could result merely from humans -- and captive gorillas -- living longer, Austad said.
"It's going to make evolutionary biologists think long and hard about what this suggests for humans," Austad said. "Right now, they're saying humans are unique. It may turn out you can get gorillas to live 75 years, and 25 years of that is post-menopausal."
This isn't entirely new, but it is apparently a nice survey of older known-age gorillas, which is the best sample available for it. According to the article, the average age of the post-menopausal gorillas is 44.
How Hamilton mathed up senescence
This is one of the most beautiful openings to a paper, ever:
Consider four hypothetical genes in man. Suppose all are limited in their expression to the female sex and also age-limited in the following way: each gives complete immunity against some lethal disease but only for one particular year of life. Suppose the first gives immunity for the first year, the second for the fifteenth, the third for the thirtieth, and the fourth for the forty-fifth. What are the relative selective advantages of these genes?
If for further simplicity parental care is ignored and it is assumed that the menopause always comes before age 45, it is at once obvious that the fourth gene is null, whereas all the others do confer some advantage. It is also fairly obvious that the third gives less than the second. But how much less? Does the second give a maximum becasue it occurs at the age of puberty? Does the first give less than the second?
The importance of questions of this kind for an evolutionary theory of senescence has been realized for some time. Most of the answers that will be given in this paper agree with the theory of Williams (1957). Although perhaps not obvious, they are so simple that it is surprising to find almost no indication that they had been realized earlier. Several writers have in effect answered the last two questions in the affirmative, which is for the one inexact and the other wrong.
If anybody in biology ever wrote like Nero Wolfe talks, it was Bill Hamilton. That intro is from "The Moulding of Senescence by Natural Selection," (Hamilton 1966:12-13), which ought to be required reading, if it isn't.
Later in the paper Hamilton presents almost fully-formed his idea of "sibling replacement" to explain why subadult mortality should be concentrated in infants:
Suppose that the catching of a disease in the immature period is ineveitable and that hte first infection has only two possible outcomes: death or survival with perfect immunity against second infection; and suppose that the probabilities do not change according to the age of the first infection. Then if there is any degree of sibling replacement at all, a gene bringing forward the expected age of first infection will be selected, for it can easily be seen that the more commonly the gene is appearing in a progeny the larger its expected completed size will be, while at the same time the expected frequency of the gene within the progeny is unchanged.
If the bringing forward of the susceptibility involves a disadvantage, for instance by a slight increase in the chance that death is the outcome of infection, the situation is more complex and will require mathematical analysis to delimit the possibilities. This is because it is then no longer true that the proportion of the gene is unchanged by the amount of replacement that goes on; positive selection could fail even if it was guaranteed that the amount of replacement could more than compensate for the extra mortality. This is in effect a problem of a more "altruistic" versus a more "selfish" trait (ibid:39).
And so the theoretical power of inclusive fitness is made plain: it encompasses even death itself in the service of first-order relatives.
Paging Randy Newman...
If "short people got no reason to live", then why exactly do they live longer than tall people?
This study (abstract) from 2003 reviewed evidence for the relationship between stature and longevity, finding that short people have a substantial record of living longer in many large-population and some more select samples:
Findings based on millions of deaths suggest that shorter, smaller bodies have lower death rates and fewer diet-related chronic diseases, especially past middle age. Shorter people also appear to have longer average lifespans. The authors suggest that the differences in longevity between the sexes is due to their height differences because men average about 8.0% taller than women and have a 7.9% lower life expectancy at birth. Animal experiments also show that smaller animals within the same species generally live longer.
The paper is one of those reviews of dozens of studies, so there are lots of references. Here's an interesting factoid:
In addition, centenarians tend to be quite short and light [14, 63 and 69]. Japanese centenarians averaged about 10 cm shorter than 75 year olds and Hungarian centenarians averaged 154 cm. In an unpublished analysis, we compared 14 European countries divided into taller and shorter halves based on heights during youthful years and found the shorter countries averaged 77 centenarians per million vs 48 per million for the taller half. Short Sardinians and Okinawans, not included in this analysis, also have exceptionally high percentages of centenarians (136 and 340 per million respectively).
They also did a survey of famous dead people to see if the taller ones died sooner (they did). I wonder if that included the relatively short and long-lived John Quincy Adams, incidentally, the first president to wear long pants instead of knee britches (!). In fact, looking over the numbers, the dividing point for "short" famous people is 173 cm, or 5 feet 8 inches, which is a bit taller than average height for men.
The authors also suggest that the added longevity due to caloric restriction in experimental animals may actually be a reflection of small body size, rather than of caloric restriction per se. Their preferred explanation is called the "entropy theory" of aging, which essentially is the argument that the bigger you are, the more things can go wrong (Samaras 1974).
My major complaint is that more of the original data are not plotted -- there are a lot of plots of group means. But without seeing the variance in the data, it is impossible to tell if the effect of size comes from a large effect on a subset of very tall people, or a broad regression of longevity against size. In fact, I would strongly suspect that there is some optimum height that has the longest lifespan, with shorter lifespans on either side. This is almost certainly true, since congenital dwarfs do not have as long an average lifespan as nondwarfs. But the issue is where the optimum size may be -- is it relatively high within the range of, say, 5' 5" to 5' 8"? Or is it low, say, 4' 6" to 4' 10"?
Evolution of height?
Of course, this is one of those basic size questions that has a lot of impact on human evolution. For one thing, people today really vary in height in different populations. Do relatively tall populations pay a cost in longevity. The study suggests that at least in developed societies, they do. But how do pygmies compare? This kind of question may not currently be answerable, considering that differences in mortality rates in human populations owe much more to infectious agents than to anything else.
Rephrase the question, then: considering that mortality rates during recent human evolution were much higher (and average lifespan much shorter) than today, do the height differences in longevity that we now observe have any evolutionary relevance at all? It is hard to argue that their effect should have been the same as today. But on the other hand, it is hard to believe that radical size differences between populations had no effect on life history evolution (and longevity) at all. The question is how much effect, and how relevant the example of recent human demography.
Then there are the body size changes in the fossil record. Conventionally, we think that the increase in body size from Homo habilis (or a like-sized variant of early Homo) to early humans was accompanied by a substantial increase in body size (evidenced in particular by early human fossils like Nariokotome [KNM-WT 15000], KNM-ER 3228, and KNM-ER 1808). Conventionally, we also tend to think that lifespan increased at this time, along with body size. But the negative relation of body size on longevity in living humans (and possibly other mammals) creates an evolutionary challenge: if both longevity and body size increased (and substantially so in both instances), then some of the genetic changes accompanying this shift must have been under strong antagonistic selection -- pressure to find ways to eke greater lifespan out of larger animals.
Or how about Neandertals and later Europeans? The Neandertals were not taller, but they were bigger. Which is more important? The evidence suggests that Upper Paleolithic people had much higher lifespans than Neandertals. Could this have been a consequence of their smaller bodies? Or did it occur in spite of their greater height? And did the non-European contemporaries of Neandertals, many of whom were presumably smaller than Neandertals, possibly live longer? If so, such a life history difference may have been fundamental to the evolution of modern humans.
Lots of interesting possibilities. It is unclear right now to me whether the size of the size-longevity effect is great enough to account for many of these things (or in the case of early Homo, to affect it markedly). But an 8 percent difference in both size and longevity between men and women does indicate that the effect may well have been on the scale of evolutionary importance.
References:
Samaras TT. 1974. The law of entropy and the aging process. Hum Develop 17:314-320. Abstract
Samaras TT, Elrick H, Storms LH. 2003. Is height related to longevity? Life Sci 72:1781-1802. PubMed
Is life history invariance an illusion or not?
I posted last year about a paper in Science by Sean Nee and colleagues, which showed that the idea of "life history invariants" was an illusion of flawed statistics.
The theory of invariants in life history is mostly attributable to Eric Charnov, who also reviewed the key principles in his book, Life History Invariants : Some Explorations of Symmetry in Evolutionary Ecology. In the interim, Charnov has been kind enough to forward a short article he has in press in Oikos, which expresses some of the mathematics underlying the "dimensionless ratios", and some of the reasons they might be expected to be independent of body size.
Now, Charnov and his colleagues have a technical comment in this week's Science:
Nee et al. (Reports, 19 August 2005, p. 1236) used a null model to argue that life history invariants are illusions. We show that their results are largely inconsequential for life history theory because the authors confound two definitions of invariance, and rigorous analysis of their null model demonstrates that it does not match observed data.
Nee and colleagues have a response to the comment, which as you might expect doesn't agree:
Savage et al. describe two different kinds of invariant. The kind they claim to have the greatest biological importance allows the invariant quantities to vary widely, even randomly, between different species. We do not agree that such quantities reveal any deep constraints on evolution.
I have my own perspective on this exchange. Mostly, I come from outside the problem of life history, and my interest in it concerns one small taxonomic group -- the hominids.
Deviations from a regression cannot be used to confirm the regression. Consider Meganthropus.
References:
Charnov E. 1993. Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology. Oxford University Press, Oxford. Amazon
de Jong G. 2005. Is invariance across animal species just an illusion? Science 309:1193-1195. Full text (subscription required)
Nee S, Colegrave N, West SA, Grafen A. 2005. The illusion of invariant quantities in life histories. Science 309:1236-1239. Full text (subscription required)
Savage VM, White EP, Moses ME, Ernest SKM, Enquist BJ, Charnov EL. 2006. Comment on "The illusion of invariant quantities in life histories. Science 312:198. DOI link
Cut early mortality; cut late mortality
A PNAS paper by Eileen Crimmins and Caleb Finch finds evidence that early infection, growth, and longevity are all linked:
ABSTRACT: Using historical data from cohorts born before the 20th century in four northern European countries, we show that increasing longevity and declining mortality in the elderly occurred among the same birth cohorts that experienced a reduction in mortality at younger ages. Concurrently, these cohorts also experienced increasing adult height. We hypothesize that both the decline in old-age mortality and the increase in height were promoted by the reduced burden of infections and inflammation. Thus, early growth and cardiovascular diseases of old age may share infectious and inflammatory causes rooted in the external environment.
The paper shows that, at least in the study populations, a reduction in early mortality not only affects the early part of the life table but actually flattens the mortality throughout the lifespan to some extent. Avoiding early infections appears to have cut old-age mortality at the same time it increased early growth.
I wonder to what extent the link between early infections and later inflammation and chronic disease is a product of recent disease evolution. It's not clear, since chronic inflammations were apparently common among some (and possibly all) archaic humans. But these probably did not bear any relationship to many of the epidemic diseases that have recently caused so much childhood mortality. On the other hand, there have been some very long-lasting ones -- tuberculosis comes to mind, as one that can have far-reaching infectious consequences in the body and has a long evolutionary association with humans.
References:
Crimmins EM, Finch CE. 2006. Infection, inflammation, height, and longevity. Proc Nat Acad Sci USA Online before print. Abstract
Bringing Kurzweil's dream to earth
I've seen a lot of attention to the new Ray Kurzweil book, Fanstastic Voyage: Live Long Enough to Live Forever, but only now have I seen a review by someone knowledgeable about the evolutionary biology of aging. Tom Kirkwood is just such a person, and Nature has his review of the book, along with another book on the same topic (by Philip Lee Miller and the Life Extension Foundation, with Monica Reinagel --- does that sound like a 70's funk band, or what?).
The review is basically supportive of the actual content of the books, but at the same time critical of the hype. Here's a sample:
Peel away the gloss, however, and these two books turn out to be rather humdrum contributions to the growing genre of 'how to' manuals that aspire to tell us "how to benefit from cutting edge science and add years to your life" and "how to extend the prime of your life and rejuvenate your body, mind and spirit". Both books do a fair job of summarizing the current state of knowledge about factors that can affect the ageing process and about what can sensibly be done to increase your chances of living into old age in good health.
And there is this interesting passage:
We know, for example, that, in model organisms, boosting some of the mechanisms for cellular maintenance and repair can indeed extend life-span. This does not mean that the same techniques will necessarily work in humans, because we know from comparative studies that humans are already endowed, for good evolutionary reasons, with much better maintenance systems than shorter-lived species. By analogy, a design modification that boosts the performance of my own modest car will not necessarily make a Maserati go faster, as the Maserati is engineered for peak performance already. But we can try.
One might say the best thing about immortality is getting to see the full effects of compound interest. But don't bet on it yet.
References:
Kirkwood T. 2005. Live long and prosper (combined review). Nature 436:915-916. Full text (subscription required).
Genetics of the superfertile
Reuters reports on a research study by Dr. Neri Laufer (Hadassah University Hospital, Jerusalem) into the genetic variation underlying fertility in older women. The newsworthy finding is the identification of a "select group of genes" that influence late fertility:
Using gene chip technology, [Laufer] and his team compared the genetic profiles of eight women chosen from 250 who had had children past the age of 45 with profiles of six others who had finished their families by the age of 30.
"These women appear to differ from the normal population due to a unique genetic predisposition that protects them from the DNA damage and cellular aging that helps age the ovary," he said.
Conceiving naturally past the age of 45 is rare because a womanÕs supply of eggs diminishes as she ages and approaches the menopause, which normally occurs around the age of 50.
The report implies that the alleles may be more common in some groups than others. Although it does not say, the geographic extent of the samples was almost certainly limited, so the following cannot be considered conclusive, but it is interesting:
All the super-fertile women in the study were Ashkenazi Jews, descended from the Jewish communities of central and eastern Europe. Most had had six or more children, did not use contraception and had a low miscarriage rate.
"They challenged their reproductive system until the menopause," said Laufer, who added that the distinct genetic fingerprint was not unique to them.
He found a similar profile in Bedouin women who also had children late in life.
It might be highly localized, it might be global. Whichever is the case, this is certainly interesting from the standpoint of the evolution of life history traits in humans. The persistence of fertility into later adulthood would seem to be highly adaptive, unless the allele has some cost for earlier survival or reproduction. The distribution of the allele and that of linked loci could tell us if it has been recently spreading, or if it is an ancient polymorphism. To my knowledge, this is the first examination of the determinants of fertility late in life, as opposed to genetic determinants of mortality. The shape of human life histories is affected by selection on both, so this is an important step.
Life history invariants: broken beyond repair?
Here's a study that won't be reported in the science press, but is much more important to evolutionary theory than anything else I've read this month.
Sean Nee and colleagues write in the August 19 Science that attempts to construct an overarching theory of animal life history evolution may be written off because of a fundamental methodological error.
The problem comes down to a simple error in interpreting log-log plots.
Here's the abstract:
Life-history theory attempts to provide evolutionary explanations for variations in the ways in which animal species live their lives. Recent analyses have suggested that the dimensionless ratios of several key life-history parameters are the same for different species, even across distant taxa. However, we show here that previous analyses may have given a false picture and created an illusion of invariants, which do not necessarily exist; essentially, this is because life-history variables have been regressed against themselves. The following question arises from our analysis: How do we identify an invariant?
The development of the idea of "invariants" in life history is due to Eric Charnov (reviewed in Charnov 1993). The idea is that if you examine the ratio of two dimensions of life history -- for example, the ratio of maturation age to average adult life span -- that the ratio is constant across species. If this were true, then a major aim of life history theory would be to explain why these invariant ratios have the values they do. Presumably, the ratios found across animal species would reflect ecological trade-offs -- for example, bigger animals require more time to develop, and therefore must extend their adult life span proportionately longer to allow for the risks of juvenile mortality, costs of investing more in offspring, or some other constraint.
The idea of invariants is not derived from theory -- it is an argument based on empirical observations. When you plot an life history traits from different species against another trait, in many cases you find that the logarithm of one is linearly related to the logarithm of the other, with a slope very near 1.0. This would be precisely the relationship you would expect if the ratio between the two traits were constant.
What Nee and colleagues demonstrate is that the converse is not true. Although an invariant ratio does lead to a log-log slope near 1.0, a log-log slope near 1.0 may result from many relationships other than an invariant ratio. In particular, a random set of ratios will still generate a log-log slope near 1.0.
A commentary by Gerdien de Jong (subscription required) explains the paper.
But Nee et al. (2) describe the general rationale of how slopes of 1 at high R2 arise in log-log plots, independent of the distributions of the traits. The culprit is a variable on the y axis that is a fraction of the x-variable: The plot is of y = cx, with c < 1. In a log-log plot of cx versus x, a slope of 1 follows automatically. A wide range on the x axis--from rabbit to whale--guarantees a high R2. The evidence for life history invariants vanishes as the method of finding them evaporates (de Jong 2005:1194).
Why does this happen? Simply put, a short-lived species must have a shorter maturation age than its average life span, but not too much shorter. The slope of 1.0 comes from this fact alone: one variable is constrained to be close to the other, owing to the fact that it is some substantial proportion of that other variable.
Why should the correlation be high? The answer to this should be familiar to any paleontologist: it's a mouse to elephant curve. The independent variable ranges across so many orders of magnitude that the variance about the regression essentially disappears.
The essential emptiness of the theory arises here:
The most notable invariants are typically taken to be those that hold over several orders of magnitude of variation in the value of the biological characters; we now see that it is this wide variability of the characters that inevitably makes the invariants notable (Nee et al. 2005: 1238).
When I read through Charnov's book (Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology), it was with an eye toward the relationship of average life span to maturation age. Personally, I found the log-log plots less than convincing, because there was too much variation hidden in them. A 0.95 correlation on a log-log plot across primates still allows individual values to vary by a lot, just because a log-log plot appears to smash the variation down so much.
This study attacks the basis of the theory much more directly:
From the time of the introduction of invariants, many other studies and discussions have accepted their existence on the basis of these sorts of demonstrations and attempted to explain them theoretically or infer their consequences. For example, in his review of the canonical monograph on life-history invariants (1), Maynard Smith refers to the M/b data we have just discussed and says "M/b is approximately constant (0.2) for species as different as the tree sparrow and wandering albatross"(31). This is in spite of the fact that the data to which he is referring show the ratio varying between 0.1 and 0.5. Maynard Smith was not the only reviewer to accept that this ratio is constant (32), and the status of these life-history invariants is such that they have now found their way into the popular physics literature (33). In fact, in a population of constant size, the ratio M/b is, essentially, the probability of surviving from egg to breeding age and therefore is constrained to be between 0 and 1 (Nee et al. 2005: 1238).
This was certainly my perception for the primates. There was a strong claim that the values of interest were invariants, despite the fact that the data themselves show fairly wide variation in the actual ratios.
What is the solution to this problem for life history theory? Nee et al. suggest comparisons with other dimensionless values; de Jong suggests a direct examination of fitness relations in different species. The latter approach seems the most likely for hominoids, although this essentially amounts to a species-specific examination in each case.
What I wonder is whether other kinds of relations -- ones we may be more familiar with -- may prove to be manifestations of the same error. I'm going to be looking through some papers in the next few days with that in mind.
References:
Charnov E. 1993. Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology. Oxford University Press, Oxford.
de Jong G. 2005. Is invariance across animal species just an illusion? Science 309:1193-1195. Full text (subscription required)
Nee S, Colegrave N, West SA, Grafen A. 2005. The illusion of invariant quantities in life histories. Science 309:1236-1239. Full text (subscription required)
Get ready, we're getting older
The Scientist has a very nice article titled "The Longevity Dividend", about attempts to treat diseases of aging with preventative biotechnology.
Some people, including a proportion of centenarians, live most of their lives free from frailty and disability. Genetics plays a critical role in their healthy survival. Identifying variation in these subgroups of humans holds great potential for improving public health. For example, microsomal transfer protein (MTP) on chromosome 4 has been identified as a longevity modifier in a sample of centenarians; there is strong evidence linking a common variant of KLOTHO, the KL-VS allele, to human longevity; and it has been demonstrated that lipoprotein particle sizes promote a healthy aging phenotype through codon 405 valine variation in the cholesteryl ester transfer protein (CETP) gene.
The article argues that the aging population may yield a "dividend" in the form of greater productivity, but only if research can succeed in preventing or allaying the disabilities of aging.
Mandrill reproductive variance
Joanna Setchell and colleagues (2005) present observations on the sexual competition and reproductive success in mandrills. For a quick primer on mandrill social interactions:
Mandrills (Mandrillus sphinx, Cercopithecidae) live in multi-male, multi-female groups, and are one of the most sexually dimorphic species of land mammal, typifying the sex differences that prompted Darwin to develop his theory of sexual selection. Male body mass is 3.4 times that of females (Setchell et al. 2001), and male canine teeth measure 44 mm, versus 10 mm in females (Setchell and Dixson 2002; Leigh et al. 2005). Adult males also possess a variety of exaggerated secondary sexual adornments, including brightly coloured skin on the face, rump and genitalia; boney supra-maxillary swellings; a yellow beard; a long cape of hair and an epigastric fringe of white hair (Hill 1970). This adult sexual dimorphism is reflected in patterns of growth and development: while females reach adult size at the age of 7 year, males do not attain adult size and appearance until 9-10 year (Setchell et al. 2001; Setchell and Dixson 2002). Differences between males and females are thought to have evolved due to intense male-male competition in this species (Wickings and Dixson 1992b; Setchell and Dixson 2001), although female choice for large, ornamented males may also be involved (Setchell 2005).
The study kept track of reproduction and mortality in a captive population of mandrills. So it doesn't exactly replicate wild population dynamics, but the results are still striking in showing strong difference between males and females.
Mortality was generally low, but a marked sex difference was observed (Fig. 1; log-rank test statistic=11.44, df=1, p<0.001). The two sexes were indistinguishable until the age of 4 year, but sex differences became marked at 6 year. Of 111 females, only eight disappeared (7%): seven before 5 year, and one after 19 year. Females lived to 22+-1 year (95% CI 21-24 year, median survival could not be calculated for females, due to the small number of disappearances), although the data were limited to 25 year, meaning that females may survive longer than this. Male survival was 14+-1 year (95% CI 13-16 year, median 17 year); no male lived longer than 20 year. Males that disappeared prior to reaching adulthood (n=14) simply disappeared from one day to the next. However, of the 10 adult males that disappeared, four were seriously wounded prior to disappearance (likely as a result of male-male combat); three of these were alpha male at the time.
This is in captive enclosures totalling less than 10 ha. In other words, the males are pretty rough on each other. And it has results: reproductive variance is many times higher in males than in females -- up to 10 times higher including males who died without reproducing. Female reproductive variance may be understated by the study, since there is little or no predation, little infant mortality, and the population is growing -- all these should tend to make females more equal in their reproductive success.
But the age distribution of reproduction is the most impressive result:
Reproduction vs. age in mandrills, from Setchell et al. (2005)
Overwhelmingly, alpha males have almost all the offspring, and they fall into a limited class of ages. They have to be big enough (and experienced enough), and they have to be healthy and strong enough. And when they aren't, they're out.
Nine males attained top (alpha) rank during the study period. Males gained alpha-status between the ages of 9 and 14 year, with the exception of a 4-year old who had no competing adult male. Males that survived longer were thus significantly more likely to become alpha (logistic regression: alpha vs. non-alpha, B=0.38, standard error=0.12, Wald statistic=10.66, df=1, p=0.001, Exp(B)=1.46). However, of the 22 males that reached adulthood and could potentially attain alpha status, only nine (41%) did so, while only four of ten males (40%) that reached 15 years (older than the oldest male that became alpha) became alpha during their career. Tenure as dominant male varied between 1 month and 6 year (mean 34+/-9 months, median 24 months).
Attaining alpha rank had a clear influence on reproductive output (Fig. 5), and alpha males sired 85% of offspring (163 of 193 resolved paternities). Alpha males sired up to 13 infants in any one year, versus a maximum of four infants for non-alpha males.
Not unexpected, but startling in the intensity of competition.
References:
Setchell JM, Charpentier M, Wickings EJ. 2005. Sexual selection and reproductive careers in mandrills (Mandrillus sphinx). Behav Ecol Sociobiol 58:474-485. DOI link
Longer life with younger mothers
This NIH study reported by E. J. Mundell is curious:
Society's oldest members are most likely to be born to its youngest mothers, new research suggests.
The odds of living to 100 and beyond double when a person is born to a woman under 25 years of age, compared to those people born to older mothers, according to one of the most rigorous studies on the subject yet conducted.
The study considered some other factors besides maternal age also:
But what other factors encourage "extreme" old age? Previous research by Gavrilov and his wife/co-researcher, Natalia Gavrilova, has uncovered some clues. For example, in research published over the past few years, they found that U.S. centenarians were more likely to come from farming families in the Midwest than from any other demographic.
They also discovered that being the first-born in a family meant a lot, boosting the odds of making it to 100 by nearly 80 percent.
"But nobody knew why that was -- sometimes in research you get answers, but you also get new questions," Gavrilov said.
So, he and his wife set out to solve that puzzle. They selected 198 centenarians from across the United States, checking and double-checking their ages using every form of documentation available. Comparing the centenarians' histories to those of their siblings, the researchers then analyzed the data to help explain the "first-born effect."
One theory -- that first-born children might have been relatively protected from pediatric illness because they weren't surrounded by disease-bearing siblings in infancy -- didn't pan out. "We found that even at age 75 it still matters that one is first-born," Gavrilov said. "It's a late-life phenomenon."
A second theory -- that first-born kids reaped the benefit of a relatively young, strong and productive father -- also fell flat. "We got the very clear result that the father's age wasn't important," the Chicago researcher said.
That wasn't the case for mothers. In fact, statistical analysis revealed that young maternal age at birth completely accounted for the first-born effect.
This is good reporting to keep these different hypotheses straight and explain why the data supported one instead of others.
Although the new research shows no effect for paternal age on survivorship in these offspring, an earlier study by the same authors found that paternal age made a lot of difference, at least considering the longevity of their daughters. Here is part of the abstract of Gavrilov et al. (1997):
The daughters born to old fathers 50 - 59 years lose about 4.4 years of their life compared to daughters of young fathers 20 - 29 years and these losses are highly statistically significant, while sons are not significantly affected. Since only daughters inherit the paternal X chromosome, this sex-specific decrease in daughters' longevity might indicate that human longevity genes (crucial, house-keeping genes)sensitive to mutational load might be located in this chromosome.
But this study was of historical families of aristocrats, so maybe they were missing some effects that are being caught in the study of centenarians. Or maybe paternal age used to make a difference and doesn't anymore? In any event, it's curious. If this were "mutation load" or other genetic effects, I would expect the age of both parents to make more of a difference. And the combination of older fathers and older mothers may have changed over the years, which adds another complication with respect to mutational effects. This may be a tough one to work out.
References:
Gavilov LA and 8 others. 1997. Mutation load and human longevity. Mut Res 377:61-62.
The mystery of the 8-year orangutan birth interval
Reading through some primate literature, I found this paper really interesting:
Development of Ecological Competence in Sumatran Orangutans
Maria A. van Noordwijk and Carel P. van Schaik
Data on orangutans (Pongo pygmaeus abelii) living in a Sumatran swamp forest yield an estimated median interbirth interval of at least 8 years, concurring with findings from other sites. This longest known mammalian interbirth interval appears due to maternal amenorrhea during the long exclusive dependence of the offspring. We describe the development of various components of offspring independence. In this arboreal ape, 3-year-olds had largely reached locomotor independence. Nest-building skills were also well-developed in 3-year-olds, but immatures shared their motherÕs nest until weaned at around age 7. At time of birth of the new sibling, association with the mother had begun to decline
for both male and female offspring, suggesting that the immatures had mastered all the necessary skills, includ- ing basic tool use, to feed themselves. By about 11 years of age, they also ranged independently from the mother. These results show that orangutans do not develop independence more slowly than chimpanzees. Why, then, is weaning 2 years later in orangutans? In chimpanzees, mothers are often accompanied by two or even three consecutive offspring, unlike in orangutans. This contrast suggests that an orangutan mother cannot give birth until the previous offspring is ecologically competent enough to begin to range independently of her, probably due to the high energy costs of association. Thus, the exceptionally long interbirth intervals of orangutans may be a consequence of their solitary lifestyle.
Sure, first of all as a father of young children, I must say reading "weaned at around age 7" made my jaw drop.
But mainly, orangutans stand out as a puzzle in comparison to other hominoids because of this extremely long birth interval. Eight years between offspring is just tremendous, compared to 5-7 years in chimpanzees --- or more shocking, 3-4 years in early humans.
Of course, these are well-known facts, always useful to surprise undergraduates (you mean, humans are r-selected?!). The interesting part of the new paper is the test of why orangutan birth intervals are so long.
The paper finds that juvenile orangutans develop toward independence at basically the same rate as chimpanzees. But orangutan mothers do not have more than a single young offspring accompanying them at a time:
This study showed the following pattern in infant development of wild orangutans. Around age 3, infants approach locomotor competence (although they still need help to cross major gaps), can build nests and protect themselves against rain, and begin to spend time in another tree than that of their mother. The next major change occurs at time of weaning, around age 7, when mothers stop playing with their offspring and occasionally become less tolerant around food, the youngsters sleep in their own night nest, and proximity ( 10 m) begins a precipitous decline. At this age, the weanling has already achieved an adult-like activity budget, and, by definition, foraging competence. Around the time the next infant is born, association time ( 50 m) declines steeply to reach adult levels at around age 10 or 11, indicating that immatures at that age have also achieved ranging competence. Thus, consecutive infants overlap only briefly in their association with the mother (Noordwijk and van Schaik 2005:89).
The proposed reason is subtle. It is not that there is insufficient energy to support multiple offspring; it is that supporting a juvenile longer is more necessary for a solitary ape than for an ape living in a group. Staying with the mother allows juveniles to avoid predation and have help foraging effectively until they are ready for complete independence.
This hypothesis has a clear corollary: if orangutans have long birth intervals because they are solitary, then other apes (and humans) may have short intervals because they are social. It is not at all clear that short birth intervals --- even chimpanzee-length ones --- are the ancestral condition for hominoids.
Under competition from cercopithecoids, who reproduce much faster than apes, there would have been strong incentives for today's hominoid lineages to have shortened birth intervals. If group life allows both shorter birth intervals and more social learning, this combination may have been the only way that the African apes survived.
If so, now-extinct Miocene apes may have had life histories more like orangutans than like other living apes.
References:
van Noordwijk MA and van Schaik CP. 2005. Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79-94.
Overweight is best?
The New York Times reports a new study in JAMA on the mortality risk associated with different BMI classes. The study found that obesity and underweight classes faced a higher mortality risk, but that overweight people were just as well off as normal weight.
In our analysis, we did not find overweight (BMI 25 to <30) to be associated with increased mortality in any of the 3 surveys. Our results are similar to those of a previous analysis of NHANES I and II data that found little effect of overweight on life expectancy. Our finding is consistent with other results reported in the literature, although methodologic differences often preclude exact comparisons. In many studies, a plot of the relative risk of mortality against BMI follows a U-shaped curve, with the minimum mortality close to a BMI of 25; mortality increases both as BMI increases above 25 and as BMI decreases below 25, which may explain why risks in the overweight category are not much different from those in the normal weight category (Flegal et al. 2005:1866).
The authors speculate that there may have been a recent reduction in mortality associated with obesity and overweight because of increasingly successful treatment of chronic high blood pressure and high cholesterol. Likewise people with extra weight may have an advantage in maintaining bone density and muscle strength into old age compared to normal or underweight people.
References:
Flegal KM, Graubard BI, Williamson DF, Gail MH. 2005. Excess deaths associated with underweight, overweight, and obesity. JAMA 293:1861-1867. JAMA Online
Two interesting things about postreproductive lifespans
First, this:
Consider first an astonishing fact. Female life expectancy in the record-holding country has risen for 160 years at a steady pace of almost 3 months per year [Fig. 1 and suppl. table 1 (1)]. In 1840 the record was held by Swedish women, who lived on average a little more than 45 years. Among nations today, the longest expectation of life--almost 85 years--is enjoyed by Japanese women [HN2]. The four-decade increase in life expectancy in 16 decades is so extraordinarily linear [r2 = 0.992; also see suppl. figs. 1 to 5 (1)] that it may be the most remarkable regularity of mass endeavor ever observed. Record life expectancy has also risen linearly for men (r2 = 0.980), albeit more slowly (slope = 0.222): the gap between female and male levels [HN3] has grown from 2 to 6 years (suppl. fig. 2) (Oeppen and Vaupel 2002:1029).
The countries change, but the pattern continues. Older and older.
Then this:
The trajectories [according to which mortality decelerates with age] differ greatly. For instance, human mortality at advanced ages rises to heights that preclud the longevity outliers found in medflies. Such differences demand explanation. But the trajectories also share a key characteristic. For all species for which large cohorts have been followed to extinction, mortality decelerates and, for the biggest populations studied, even declines at older ages. A few smaller studies have found deceleration in additional species. For humans, the insects, and the worms, the deceleration occurs at ages well past normal reproductive ages.
If older individuals contribute to the reproductive success of younger, related individuals, then they promote the propagation of their genes. Hence, in social species, the effective end of reproduction may be much later than indicated by fertility schedules. The deceleration of human mortality, however, occurs after age 80 and the leveling off or decline after age 110, ages that were rarely if ever reached in the course of human evolution and ages at which any reproductive contribution is small (Vaupel et al. 1998:858).
References:
Oeppen J, Vaupel JW. 2002. Broken limits to life expectancy. Science 296:1029--1031. DOI link
Vaupel JW et al. 1998. Biodemographic trajectories of longevity. Science 280:855-860.
Hunter-gatherer mortality
Kim Hill and colleagues (2007) report in the current Journal of Human Evolution on the mortality profile of recent Hiwi hunter-gatherers. Here is their abstract:
Extant apes experience early sexual maturity and short life spans relative to modern humans. Both of these traits and others are linked by life-history theory to mortality rates experienced at different ages by our hominin ancestors. However, currently there is a great deal of debate concerning hominin mortality profiles at different periods of evolutionary history. Observed rates and causes of mortality in modern hunter-gatherers may provide information about Upper Paleolithic mortality that can be compared to indirect evidence from the fossil record, yet little is published about causes and rates of mortality in foraging societies around the world. To our knowledge, interview-based life tables for recent hunter-gatherers are published for only four societies (Ache, Agta, Hadza, and Ju/'hoansi). Here, we present mortality data for a fifth group, the Hiwi hunter-gatherers of Venezuela. The results show comparatively high death rates among the Hiwi and highlight differences in mortality rates among hunter-gatherer societies. The high levels of conspecific violence and adult mortality in the Hiwi may better represent Paleolithic human demographics than do the lower, disease-based death rates reported in the most frequently cited forager studies.
The mortality rates reported for the Hiwi are higher than those for other hunter-gatherers -- especially the African groups (Hadza and !Kung), but not stunningly so. Among pre-1960 Hiwi males, 57 percent could expect to survive to age 15, and 43 percent to age 30, with an average young adult mortality rate of around 2 percent annually. So it is not anything like as high as has been suggested for Neandertals and earlier humans (with annual mortality rates as high as 6 percent).
The most interesting aspects of the paper are the comparisons between the Hiwi and other ethnographically-known hunter-gatherers. Many of the differences in mortality profiles are attributable to strong cultural differences:
Cause of death among the groups differs considerably. Disease is an important cause of death in all groups, but represents only 20% of deaths in the precontact Ache, 45% among the precontact Hiwi, and about 75â85% of all Hadza, !Kung, and Agta deaths. Respiratory disease is the main killer of the Ache, whereas gastrointestinal pathogens are most important among the Hiwi and probably Hadza. Among the !Kung, respiratory and gut infections are about equally important. Violence is the major cause of death among the precontact Ache (55% of all deaths) and very important among the Hiwi (30% of all deaths), but notably less important in the two African societies and the Agta (3â7% of all deaths). Indeed, the crude homicide/warfare death rates per year lived are more than ten times higher among the Hiwi and Ache than among the Hadza or !Kung (1/100 and 1/200 per year for precontact Hiwi and Ache, respectively, vs. 1/2500 and 1/3000 for the Hadza and !Kung, respectively). Blurton Jones et al. (2002) suggested that this may be due to the more pervasive effects of colonial governments in Africa and the reduction of intertribal warfare. Even so, within-group homicide and infanticide rates are also much lower among African foragers, suggesting real cultural differences in violence rates.
The most notable contrast among hunter-gatherer life tables is the overall similarity of child mortality followed by subsequent high mortality of the Hiwi and Agta in adulthood compared to the Ache, !Kung, and Hadza (Fig. 3). The number of individuals at risk in each yearly category and the number of deaths observed have been only published for the Ache and Hadza. Thus, statistical analyses of differences in mortality rates between these groups and the Hiwi can be performed using logistic regression. The results suggest that all foragers are not characterized by a single âtypicalâ mortality schedule. Analyses of the differences for infants, children, adults, and elderly using logistic regression (Table 6) shows significantly lower Ache infant mortality and early-adult mortality relative to the Hiwi, and lower Hadza adult mortality (both young and old) relative to the Hiwi. Particularly striking is the fact that Hiwi early-adult mortality rates are about double those of the Ache and Hadza (Hill et al. 2007:449-450).
Violence is as important a cause of death as disease for young Hiwi adults, and for infants as well. On page 451, the paper points out that violence and accident cause as many deaths in the Hiwi young adults as occur in most other hunter-gatherers from all causes combined. Hill and colleagues discuss this issue in relation to the possible life history pressures on Paleolithic hunter-gatherers:
If high mortality, warfare, homicide, and accidental trauma are typical of our Paleolithic ancestors, the Hiwi mortality patterns may be more representative of the past than those derived from other modern hunter-gatherers. If so, several observations about the Hiwi are important. First, conspecific violence was a prominent part of the demographic profile, accounting for many deaths in all age and sex categories. Most of the adult killings were due to either competition over women, reprisals by jealous husbands (on both their wives and their wives' lovers), or reprisals for past killings. The criollo-caused killings were motivated by territorial conquest. Moreover, infanticide (especially on females) constituted the highest mortality rate component of all Hiwi conspecific violence. Second, no predation deaths were reported despite attacks by anacondas, Orinoco caimans, and piranhas, and the presence of jaguars in the area. Accidents associated with the active-forager lifestyle were common, but disease was a more important killer, accounting for nearly half of all deaths. This suggests an adaptive landscape in which success in social relations, competitive violence, and disease resistance are paramount. This may partially explain why many of the genes that appear to have been under strong selection in the past 50,000 years affect either disease resistance or cognitive function (Wang et al., 2006), presumably related to success in an atmosphere of frequent violent social competition (Hill et al. 2007:451).
The paper also includes a substantial discussion of the implications of high young adult mortality for intergenerational investments, such as grandmothering. This is an important issue, and Hill and colleagues end their discussion with a suggestion that neither the "grandmothering" nor the "embodied capital" models for the evolution of long life spans is sufficient to explain the human pattern. In their view, the key difference between humans and other primates (notably, chimpanzees) is not life span itself, but the markedly lower mortality rate among young adults. This low mortality rate directly causes the long life span (if you don't die young, you'll live long!). Hill and colleagues favor extrinsic factors such as greater protection of children, nursing the sick, and food sharing as possible causes of reduced mortality rates in humans.
This is a thought-provoking paper, beyond the valuable data, because of its discussion. I will have more to say about the early hominids later on.
References:
Hill K, Hurtado AM, Walker RS. 2007. High adult mortality among Hiwi hunter-gatherers: implications for human evolution. J Hum Evol 52:443-454. doi:10.1016/j.jhevol.2006.11.003
Genetics and lifespan
The New York Times is carrying an article by Gina Kolata that discusses research on genetics and longevity. She has quotes from several big figures in the field -- Vaupel, Finch, Christensen -- and it's a good article.
The main idea is that lifespan is weakly heritable:
Now, Dr. Christensen and his colleagues have analyzed the data. They restricted themselves to twins of the same sex, which obviated the problem that women tend to live longer than men. That left them with 10,251 pairs of same-sex twins, identical or fraternal. And that was enough for meaningful analyses even at the highest ages. "We were able to disentangle the genetic component," Dr. Christensen said.
But the genetic influence was much smaller than most people, even most scientists, had assumed. The researchers reported their findings in a recent paper published in Human Genetics. Identical twins were slightly closer in age when they died than were fraternal twins.
But, Dr. Christensen said, even with identical twins, "the vast majority die years apart."
Basically, the argument is that death is complicated -- lots of "random" events can cause it:
The likely reason is that life span is determined by such a complex mix of events that there is no accurate predicting for individuals. The factors include genetic predispositions, disease, nutrition, a woman's health during pregnancy, subtle injuries and accidents and simply chance events, like a randomly occurring mutation in a gene of a cell that ultimately leads to cancer.
Of course, it can't be only that. After all, stature (one of the strongly heritable traits used here as a contrast) is likewise determined by disease, nutrition, mother's health, subtle injuries, and so on. It is not only the complexity, but also the size of the random component. Essentially, what is left to kill people are all the things that genes can't avoid very easily. This includes stuff that is fundamentally rare (so strength of selection is slight) as well as stuff that feeds on complexity (with multiple subsystems that can break).
There is also an interesting bit about the heritability of deaths in given age intervals -- apparently there is no significant heritability for deaths under 60. Of course, that won't be true for societies where disease causes a significant number of deaths under 60. Sure in Western Europe where you have basically sporadic cancers, heart disease and accidents, the heritability will be zero. But throw in malaria and a few disease resistance alleles, like sickle-cell, and the story will be quite a bit different. So part of the story is that we have done so well eliminating some of the main causes of mortality that interact significantly with a person's genetics.
But as the article points out, the kinds of quantification that work well for classes of people don't work so well as applied to individuals -- even identical twins. And there is some confusion there, since "heritable" doesn't mean the same thing as "identical in monozygotic twins." If you're looking for articles on genetics to give out to students, this is a good one for raising points for discussion!
Aging, telomeres, cancer and body mass
FuturePundit points me to a study of telomerase expression in mice. Here's the abstract:
In multicellular organisms, telomerase is required to maintain telomere length in the germline but is dispensable in the soma. Mice, for example, express telomerase in somatic and germline tissues, while humans express telomerase almost exclusively in the germline. As a result, when telomeres of human somatic cells reach a critical length the cells enter irreversible growth arrest called replicative senescence. Replicative senescence is believed to be an anticancer mechanism that limits cell proliferation. The difference between mice and humans led to the hypothesis that repression of telomerase in somatic cells has evolved as a tumor-suppressor adaptation in large, long-lived organisms. We tested whether regulation of telomerase activity coevolves with lifespan and body mass using comparative analysis of 15 rodent species with highly diverse lifespans and body masses. Here we show that telomerase activity does not coevolve with lifespan but instead coevolves with body mass: larger rodents repress telomerase activity in somatic cells. These results suggest that large body mass presents a greater risk of cancer than long lifespan, and large animals evolve repression of telomerase activity to mitigate that risk.
The study is discussed pretty well in this University of Rochester press release:
"Mice express telomerase in all their cells, which helps them heal dramatically fast," says Gorbunova. "Skin lesions heal much faster in mice, and after surgery a mouse's recovery time is far shorter than a human's. It would be nice to have that healing power, but the flip side of it is runaway cell reproduction -- cancer."
Up until now, scientists assumed that mice could afford to express telomerase, and thereby benefit from its curative powers, because their natural risk of developing cancer is low -- they simply die before there's much likelihood of one of their cells becoming cancerous.
"Most people don't know that if you put mice in a cage so the cat can't eat them, 90 percent of them will die of cancer," says Gorbunova.
I for one didn't know that. Of course, there is no paradox here -- early reproduction in mice has a much higher impact on their fitness than late reproduction, and they really shouldn't live long enough to compete reproductively with their daughters -- if they can devote that late reproductive effort to earlier reproduction, they certainly should do so.
But isn't it interesting that cancer in particular should be a high risk for late-living mice, and that it might be linked to the facility for healing early injuries?
Telomerase has long been recognized as one of the big baddies behind most cancers. Here's a paragraph from a 2001 review by Shay and colleagues:
Telomerase, a eukaryotic ribonucleoprotein (RNP) complex (26-33), helps to stabilize telomere length in human stem cells, reproductive cells (34) and cancer cells (35,36) by adding TTAGGG repeats onto the telomeres using its intrinsic RNA as a template for reverse transcription (37). Telomerase activity has been found in almost all human tumors but not in adjacent normal cells (35,36). The most prominent hypothesis is that maintenance of telomere stability is required for the long-term proliferation of tumors (38-42). Thus, escape from cellular senescence and becoming immortal by activating telomerase, or an alternative mechanism to maintain telomeres (43), constitutes an additional step in oncogenesis that most tumors require for their ongoing proliferation. This makes telomerase a target not only for cancer diagnosis but also for the development of novel anti-cancer therapeutic agents.
The study of telomerase knockout mice has shown that they get messed up in some ways characteristic of aging (e.g., grey hair, hair loss) and that they start having wounds in places with chronic mechanical stresses, like the distal limbs, snout, and throat (Rudolph et al. 1999). Additionally, old telomerase deficient mice had slow wound healing. In contrast, they did not suffer generalized effects of aging to other organ systems -- the effects seem to be concentrated in the skin. This makes some sense because the skin functions by attrition -- constantly wearing off into the environment and fixing itself based on environmental insults. The other system that depends on constant loss, the blood, was also affected by the lack of telomerase, with the rate of blood cell replenishment significantly lower in older telomerase-knockout mice.
Kim and colleagues (2002) presented a good review of the relation of telomeres to cancer and aging, and mention the relation to wound healing from several different studies. It's a good review of the literature to that point, and they also discuss a number of other proteins besides telomerase that are associated with maintaining telomere structure or function.
The evolution of telomere stabilization has involved multiple pathways, and that does generate an apparent paradox: a deficiency in telomerase helps to trigger certain cancers. These manage to spread by a telomerase-independent pathway, which enables cell replication to continue without telomerase. In other words, there is no single cancer switch involving telomere length, and the removal of the ordinary regulator protein may cause other pathways to spiral out of control.
References:
Kim S-H, Kaminker P, Campisi J. 2002. Telomeres, aging and cancer: in search of a happy ending. Oncogene 21:503-511. DOI link
Rudolph KL, Chang S, Lee H-W, Blasco M, Gottlieb GJ, Grieder C, DePinho RA. 1999. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96:701-712. DOI link
Seluanov A and 7 others. 2006. Telomerase activity coevolves with body mass not lifespan. Aging Cell (online early) DOI link
Shay JW, Zou Y, Hiyama E, Wright WE. 2001. Telomerase and cancer. Hum Mol Genet 10:677-685. Free full text
How modern is "modern tooth development"?
Regular readers of the blog will remember previous occasions when I have written about dental development in fossil humans. I am by no means an expert on the topic of dental development. I don't use a scanning electron microscope, or micro-CT equipment. I can recognize perikymata and striae of Retzius, but I've never counted them. I am perfectly willing to accept the idea that other people count them accurately, and even that they can determine their periodicity (that is, how many days of development each line represents).
In 2005, Guatelli-Steinberg and colleagues showed that the variation in perikymata counts for the anterior teeth of different human populations is more extensive than the differences between living people and fossil humans. I discussed that paper at the time. The perikymata counts in modern human populations are so variable, that the variation in sample means encompasses almost all fossil humans. As I noted, there are few fossil exceptions -- KNM-WT 15000 being the most important. What's worse, the variation among living people encompasses most australopithecine teeth.
To me, this was the end of the story of tooth development and maturation rates in early humans. Modern human variation encompasses most australopithecines? End of story.
So I was surprised to see last week's paper by Tanya Smith and colleagues (2007) claiming that the Jebel Irhoud 3 dentition was the earliest example of "modern" human dental development. It seems pretty clear from Guatelli-Steinberg's work that there is no modern human pattern of enamel formation.
The paper deals with this problem in a surprising way. It just doesn't talk about any of the work showing extensive variation among living people!
Still, the data are clearly there, reported in Table 2, where it is obvious that there is no significant difference between Neandertals and the modern samples. Moreover, there is no significant difference between Neandertals and Jebel Irhoud 3, except for the lower canine perikymata number, which is even more different between JI3 and the recent Africans!
The real story of the paper seems to be that Jebel Irhoud 3 has an unusually long period of enamel development compared to most recent people, and also compared to Neandertals and other early humans. But since humans vary in these traits between populations more extensively than fossil Homo, this observation demands an adaptive explanation, not a phylogenetic one.
References:
Smith TM, Tafforeau P, Reid DJ, Grün R, Eggins S, Boutakiout M, Hublin J-J. 2007. Earliest evidence of modern human life history in North African early Homo sapiens. Proc Nat Acad Sci USA (online early) doi:10.1073/pnas.0700747104
Lampl M, Mann A, Monge J. 2000. A comparison of calcification staging and histological methods for ageing immature modern human specimens. Anthropologie (Brno) 38:51-62.
Guatelli-Steinberg D, Reid DJ, Bishop TA, Larsen CS. 2005. Anterior tooth growth periods in Neandertals were comparable to those of modern humans. Proc Nat Acad Sci USA 102:14197-14202. doi:10.1073/pnas.0503108102
Guatelli-Steinberg D, Reid DJ, Bishop TA. 2006. Did the lateral enamel of Neandertal anterior teeth grow differently from that of modern humans? J Hum Evol 52:72-84. doi:10.1016/j.jhevol.2006.08.001
Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628-631.
Ramirez Rossi FV, Bermudez de Castro JM. 2004. Surprisingly rapid growth in Neanderthals. Nature 428:936-939. Full text (subscription)
Mechanisms of development and body size
I'm just doing some background reading about the body size of pygmies (for both obvious and not-so-obvious reasons) and I thought it worth making a note of this quote, from last year's paper by Andrea Migliano, Lucio Vinicius, and Marta Lahr:
Finally, the data presented here show that pygmy body size evolved through earlier cessation of growth, being therefore the result of changes in late rather than early stages of growth. This explains why brain growth, which is completed years before the onset of adolescence (28), is not affected in human pygmies (29). Therefore, if Homo floresiensis is a dwarfed form of Homo erectus, as proposed in ref. 29, the evolution of small body size on Flores could be understood as the life history consequence of ecological conditions in islands, such as increased extrinsic mortality rate and reduced resource availability (30); however, its small brain size and low encephalisation require the postulation of different adaptive mechanisms affecting earlier stages of development.
That's the concluding paragraph of what is a very nicely-done study of mortality and fertility in pygmy populations. It came out the during the acceleration press flurry in December, so I wasn't able to write it up at the time. It's certainly worth doing so, though.
The paper proposes that pygmy human populations are small because of a life history tradeoff. A "tradeoff" is the idea that a phenotypic change in either direction may have advantages and disadvantages, and selection may arrive at different optima in different populations.
In the case of life history and body size, both growing longer (and larger) and maturing faster (and smaller) have possible payoffs. Growing longer may have a fertility payoff, as larger size facilitates larger infants and shorter birth intervals. But maturing faster has a direct payoff of shortening the generation length -- all other things equal, an individual improves her fitness by reproducing younger.
So either younger or older maturation may enhance fitness, in some circumstances. Which will work in any given population depends on other factors -- in particular, the mortality pattern. If individuals have a high risk of death in early adulthood, delaying reproduction will be a bad strategy. In short, individuals should reproduce at 16 (or earlier) if there is a fair chance they will be dead by 25 or 30.
Naturally, everyone would rather live longer. But assuming that people can't control when they die, the only way to insure their fitness is to reproduce earlier.
This hypothesis, presented by Migliano et al., is about the proximate mechanism of evolution. The authors seem content to rely on traditional hypotheses about locomotion, nutrition, and thermoregulation to explain the ultimate causes of small body size -- "ultimate" in the sense that these may be the environmental causes of high mortality:
If our hypothesis is correct, the causes of the extremely high mortality rates among human pygmies need to be explained. It is here that the traditional hypotheses explaining the small body size of pygmies may prove useful. Although the challenges posed by thermoregulation, locomotion in dense forests, exposure to tropical diseases, and poor nutrition do not account for the characteristics of all pygmy populations, as pointed out by Diamond (5), they may jointly or partially contribute to the similarly high mortality rates in unrelated pygmy populations. We argue that the small body size of African and Asian pygmy populations evolved independently as a case of evolutionary convergence, resulting from a life history tradeoff between the fertility benefits of larger body size and the costs of late growth cessation under the circumstance of significant young and adult mortality.
The demographic data presented in the paper are sobering -- particularly the low survivorship values for pygmy populations across late childhood and early adulthood. However, I wonder how much of the early adult mortality in the pygmy demographic data is attributable to new pathogens. These are certainly important today, but they would not have been during most the time that small body size was being selected in these groups. On the other hand, ancient endemic pathogens and parasites also may contribute to those mortality numbers, and these might well have occurred at higher intensities in forest peoples across their histories.
References:
De Souza R. 2006. Body size and growth: The significance of chronic malnutrition among the Casiguran Agta. Ann Hum Biol 33:604-619. doi:10.1080/03014460601062759
Migliano AB, Vinicius L, Lahr MM. 2007. Life history trade-offs explain the evolution of human pygmies. Proc Nat Acad Sci USA 104:20216-20219. doi:10.1073/pnas.0708024105
Pregnancy loss in wild baboons
I ran across this new paper by Jacinta Beehner and colleagues, which has a very intensive sampling of pregnancy outcomes in Amboseli baboons:
Environmental conditions are a key factor mediating reproductive success or failure. Consequently, many mammalian taxa have breeding seasons that coordinate critical reproductive stages with optimal environmental conditions. However, in contrast with most mammals, baboons (Papio cynocephalus) of Kenya reproduce throughout the year. Here we depart from the typical approach of evaluating seasonal effects on reproduction and engage in a more fine-grained analysis of the actual ecological conditions leading up to reproduction for females. Our aim was to determine how environmental conditions, in combination with social and demographic factors, might mediate baboon reproduction. The data set includes all female reproductive cycles from multiple baboon groups in the Amboseli basin between 1976 and 2004. Results indicate that after periods of drought or extreme heat, females were significantly less likely to cycle than expected. If females did cycle after these conditions, they were less likely to conceive; and if they did conceive after drought (heat effects were nonsignificant), they were less likely to have a successful pregnancy. Age also significantly predicted conceptive failure; conceptive probability was lowest among the youngest and oldest cycling females. There was also a trend for high ambient temperatures to contribute to fetal loss during the first trimester but not other trimesters. Finally, group size and drought conditions interacted in their effects on the probability of conception. Although females in all groups had equal conception probabilities during optimal conditions, females in large groups were less likely than those in small groups to conceive during periods of drought. These results indicate that in a highly variable environment, baboon reproductive success is mediated by the interaction between proximate ecological conditions and individual demographic factors (Beehner et al. 2006:741).
So even though baboons aren't seasonal, their reproductive success varies by season. And that last part, about group size depressing conception probability, is very interesting. The paper discusses it in terms of population density, and relate it also to the increase in interbirth interval exhibited among females in larger groups (Altmann and Alberts 2003):
Many mammalian studies have documented the costs of high density on female reproduction (voles, Microtus spp.: Agrell et al. 1995; European badgers, M. meles: Cresswell et al. 1992; Woodroffe and MacDonald 1995; deer mice, Peromyscus maniculatus: Eleftheriou et al. 1962; African mole rats, Cryptomys hottentotus: Jarvis 1969; house mice, Mus musculus: Ryan and Schwartz 1977). Additionally, previous work in Amboseli has shown that females living in larger groups had longer interbirth intervals (after a surviving offspring) than females in smaller groups (Altmann and Alberts 2003a). Consistent with these previous results, the current study revealed that conception rates were significantly altered by an interaction between the number of females in each group and periods of drought. Following "good" conditions (i.e., adequate rainfall for high primary plant productivity), large and small groups had almost identical rates of conception. In contrast, following "bad" conditions (i.e., drought), rates of conceptive failure increased for females in large groups (Figure 4). These results suggest that the costs of poor ecological conditions may be borne disproportionately by females living in large groups. The detrimental impact of large group size on reproduction, particularly during drought conditions, probably results from reduced foraging efficiency from scramble competition (Bronikowski and Altmann 1996; Altmann and Alberts 2003a), as found in several other cercopithecine populations (van Schaik and van Noordwijk 1988; Dunbar 1996). Increased within-group feeding competition is widely recognized as one of the main costs of group living among social mammals (Terborgh and Janson 1986; Wrangham et al. 1993; Janson and Goldsmith 1995). The ecological constraints model suggests that scramble competition limits group size because larger groups must forage further or more often to meet the energetic requirements of their members (Milton 1984; Janson 1988; Wrangham et al. 1993; Chapman et al. 1995), and previous studies on Amboseli groups have found that dry periods are associated with increased time spent foraging (Bronikowski and Altmann 1996) (.
The correlation between group size and conception probability during droughts was not super-strong (r was not reported, but there is much scatter). Still, the conception probability in the largest groups (between 22 and 25 females) was between 2 and 10 percent, while the smallest groups (between 6 and 14 females) had probabilities between 15 and 50 percent.
If we can believe that the effect was that large, it boggles the mind to think that some females tolerate it. Why don't they abandon the large groups? There are two basic alternatives -- either they can't abandon the large groups because of the local population densities, or staying in a large group has some compensatory advantages (such as decreased predation or increased mate quality). In that respect, living in small groups may be an adaptation to shortfalls. Paradoxically, the more marginal habitat may be safer in some respects during droughts. The smaller population local population density during the weter periods allows relatively higher reproductive output during the drier periods. Thus, population dynamics across time involves tradeoffs in habitat selection and group size.
References:
Altmann J, Alberts SC. 2003a. Intraspecific variability in fertility and offspring survival in a non-human primate: behavioral control of ecological and social sources. In: Wachter KW, editor. Offspring: human fertility behavior in a biodemographic perspective. Washington, DC: National Academy Press. p 140-169.
Beehner JC, Onderdonk DA, Alberts SC, Altmann J. 2006. The ecology of conception and pregnancy failure in wild baboons. Behav Ecol 17:741-750. DOI link
Family size and lifespan
After the post about education and lifespan, I noticed a different story about how large families reduce the lifespans of parents:
With data collected from the 21,684 couples and their 174,000 children, researchers concluded that increased family size was associated with decreased survival for both parents, although significantly more for mothers. According to Smith, "Larger family size was also associated with lower offspring survival, especially for later-born children. In neither case did other factors such as economic status play a role in the survival rates." He also notes that, "Our results are consistent with the idea that reproduction requires a trade-off between quality and quantity, and may help explain the evolution of menopause as a means of increasing mother survival."
That is based on a new PNAS article by Dustin Penn and Ken Smith, "Differential fitness costs of reproduction between the sexes." The sample was Utah families between 1860 and 1895.
The paper discusses the data in terms of life history theory. While I'm all in favor of life history theory, in this case, it's not clear to me that a true life history tradeoff is really in operation. For example, they find that women who have fewer than 3 children had more than a 98 percent chance of surviving a year after their last child, while women who had 12 or more children had only a 94 percent chance of surviving that year. That is an important difference, sure, but women with 12 or more children have a higher Darwinian fitness by a long shot, despite the increase in mortality risk. There's no tradeoff.
The most tradeoff-looking observation is that survivorship to age 18 is significantly lower for offspring late in the birth order in large families. So offspring born 12th or later in their families have only a 75 percent chance of living to age 18, while the 7th to 11th offspring have over an 80 percent chance. Family size and birth order confound each other in the data (is the lower survivorship of large families due to the higher mortality of high birth-order children, or vice versa?), but the observations are in the direction of a tradeoff, with further reproduction after 11 offspring apparently providing diminishing returns. But the returns are not negative, so there is still no real tradeoff.
Apparently, in 19th century Utah, the optimum fitness strategy was to have as many children as possible, no matter what. This strategy was not cost-free in terms of parental or offspring mortality, as the paper observes, but there is no way that these numbers would lead to an adaptive constraint on human reproduction, or the evolution of menopause.
But then, 19th century Utah is not characteristic of human evolutionary history, so the question is whether the direction of relationship observed in the paper would apply at the higher adult mortality rates characteristic of ancient people. Casting a higher mortality rate across all age classes would increase the tendency toward a tradeoff, and might result in reduced fitness for the largest families due to higher mortality cost.
And there is this interesting snippet:
Mothers stressed from rearing chronically ill children that require enormous investment have short telomeres for thier age, suggesting oxidative stress and cellular senescence (Epel et al. 2004).
Lots of good pregnancy cost references, in the discussion.
References:
Penn DJ, Smith KR. 2006. Differential fitness costs of reproduction between the sexes. Proc Nat Acad Sci USA (online early) DOI link
Drinking milk can give you twins?
Science Blog has a press release regarding the research of Gary Steinman on dietary influences on twinning. I'm going to cite a lenghty passage, because it's pretty interesting, and it's a press release:
[T]he women who consume animal products, specifically dairy, are five times more likely to have twins.
...
The culprit may be insulin-like growth factor (IGF), a protein that is released from the liver of animals -- including humans -- in response to growth hormone, circulates in the blood and makes its way into the animal's milk. IGF increases the sensitivity of the ovaries to follicle stimulating hormone, thereby increasing ovulation. Some studies also suggest that IGF may help embryos survive in the early stages of development. The concentration of IGF in the blood is about 13 percent lower in vegan women than in women who consume dairy.
The twinning rate in the United States has increased significantly since 1975, about the time assisted reproductive technologies (ART) were introduced. The intentional delay of childbearing has also contributed to the increase of multiple-birth pregnancies, since older women are more likely to have twins even without ART.
"The continuing increase in the twinning rate into the 1990's, however, may also be a consequence of the introduction of growth-hormone treatment of cows to enhance their milk and beef production," said Dr. Steinman.
In the current study, when Dr. Steinman compared the twinning rates of women who ate a regular diet, vegetarian diet with dairy, and vegan diet, he found that the vegan women had twins at only one-fifth the rate of women who commonly do not exclude milk from their diets.
In addition to a dietary influence on IGF levels, there is a genetic link in numerous species of animals, including humans. In cattle, regions of the genetic code that control the rate of twinning have been detected in close proximity to the IGF gene. Researchers have found through large population studies of African American, Caucasian and Asian women that blood IGF levels are greatest among African Americans and lowest in Asians. Some women are just genetically programmed to make more IGF than others. Twinning rates in these demographic groups parallel the IGF levels.
"This study shows for the first time that the chance of having twins is affected by both heredity and environment, or in other words, by both nature and nurture," said Dr. Steinman. These findings are similar to those observed in cows by other researchers, namely that a woman's chance of having twins appears to correlate directly with her blood level of insulin-like growth factor.
"Similar to those observed in cows" is NOT the way you want to refer to twin mothers, by the way. I know one twin mother who would be markedly less likely to participate in that research.
Of course, they're monozygotic, so dairy is irrelevant.
In any event, I find it quite incredible that vegan women have twins at only one-fifth the rate of non-vegans. That seems like more of a difference than 13 percent IGF differences would explain, unless there was a large variance in levels and the effect was concentrated in the upper tail. Maybe there are other dietary factors also.
As far as growth hormone dairy is involved, it ought to be possible to find that out from women who consume organic or BGH-free milk.
And now for some twin research trivia:
Previous twinning studies
Dr. Steinman found that women who become pregnant while breastfeeding are nine times more likely to conceive twins than women who are not breastfeeding at the time of conception. He also confirmed findings by others that identical twin sets are more often female than male, especially in conjoined twin sets, and that monozygotic twin sets are more likely to miscarry than dizygotic sets. Dr. Steinman also found evidence through fingerprint analysis that as the number of fetuses in a monozygotic set increases, so does the level of physical diversity among them. In his most recent study of the mechanisms of twinning prior to the new study, Dr. Steinman confirmed that use of in vitro fertilization (IVF) methods increases the incidence of monozygotic twinning -- where the transfer and/or implantation of two embryos results in three infants -- and he proposed that adding more calcium or reducing the chelating agent ethylenediamine tetraacetic acid (EDTA) in the IVF incubation media might decrease the unwanted complication.
I suppose that observation about physical diversity would predict that clones carried apart ought to be more similar in appearance than identical twins carried together.
Lion predation on elephants
I'm reading a bit about risk in large animal hunting, and I ran across an article by Dereck Joubert on elephant hunting by lions in Botswana.
Over the 4 years, we observed a total of 74 elephants killed by lions, including eleven elephants in 1993, seventeen in 1994, nineteen in 1995, and 27 in 1996, suggesting an increasing hunting success rate. All the elephants killed, with one exception, were from breeding herds (females and young). The exception was an adult bull, previously wounded by another bull, who remained alive for several days before eventually being killed by the lions. The great majority of the young elephants killed were males, and two-thirds of the kills were of elephants in the age range 4-15 years, with highest hunting success achieved for elephants aged 4-9 years (Table 1). The animals killed were commonly on the periphery of, or straggling behind, the breeding herds, with nearly half killed more than 50 m away from the main herd. Hunts were less commonly attempted on calves which were under the age of 4 years, which remained more closely associated with their mothers. Hunting success for elephants older than 4 years apparently doubled from 33% (n = 9) in 1993 to 62% (n = 61) in 1996. Many attempts to kill adults bulls were made in
1996, when we saw lions attacking elephant bulls almost nightly although only one hunt was successful. All except one of the kills were made at night, and hunts occurred more commonly on dark moon nights than when the moon was bright.
Well, hunting elephants ought to be pretty risky (otherwise, lions would do it all the time, right?). So how many lions got hurt during all these hunts?
There was a close resemblance between the methods that the lions used to hunt elephants and the technique commonly used to hunt buffalo. This tactic included first opportunistically detecting a straggler, or targeting a vulnerable member of the herd, then circling behind the selected prey. The lions then attacked by running in as a group. One or more lions leapt up onto the back or lower flanks and orientated along the spine of the prey. They then bit down on the backbone. The lion positioned highest up the spine would still be behind the ears of the elephant and just far enough back to be out of reach of the extended trunk. The elephant was then pulled down to its knees, not collapsed because of any fatal bite to the spine. Another approach involved a running hunt causing confusion and bunching of the elephant herds. This often resulted in one elephant falling or getting separated. In all cases a rear attack was employed, never a frontal attack. In one notable case, a single male lion ran at nearly full speed into the side of a 6-year-old male calf with sufficient force to collapse the elephant on its side. On only one occasion was a lion injured by an elephant in these hunts. In that case, the elephant collapsed on top of the lion. The resulting injury to the head was therefore recorded as accidental rather than as a result of a counterattack by the elephant.
OK, so the lions mostly limited their hunts to a class of most vulnerable elephants (subadults old enough to be isolated from their mothers, and inattentive to predators -- males amounted to 236 confirmed attempts versus 38 for females!). They adopted a special hunting style that they use for other dangerous large prey animals, attacking from the back by ambush. And during all these hunts (which totaled 74 kills out of 323 attempts) only one lion was confirmed injured. The paper doesn't say how serious the injury was, or if it
was eventually fatal, but elephant-falling-on-lion can't be a good situation.
Now, the relevant measure of risk in this instance is the injury rate (or even better, death rate) per successful kill. Unsuccessful attempts might fail for many reasons, including injury, but none of these unsuccessful attempts satisfy anybody's energetic requirements. So we have one serious injury per 74 kills. There may have been other injuries that weren't major enough to be observed or counted. Limiting to the one that was counted, we have a rate of serious injury of around 1.33 percent per kill; divided among the average number of lions that participated, which isn't specified.
From the elephant perspective, there appears to be a case for strategic indifference of adult males to predation on the younger males:
When these young elephants finished and called out to their families, the lions attacked. There wa