life history

The keywords to the article include, "carnivorous marsupial" and "precocious breeding." What better teaser could you possibly hope for?

Tasmanian devils are dying because of a transmissible cell line infection, or "cancer," decimating their population. In fact, in some places it's killing 9 out of 10, which is way beyond decimation.

The new paper by Menna Jones and colleagues claims that the population is evolving toward a radical life history solution to the problem: Tasmanian devils are starting to mate and have large litters after a single year, before they have a chance to succumb to the disease:

This change in life history is associated with almost complete mortality of individuals from this infectious cancer past their first year of adult life. Devils have shown their capacity to respond to this disease-induced increased adult mortality with a 16-fold increase in the proportion of individuals exhibiting precocious sexual maturity. These patterns are documented in five populations where there are data from before and after disease arrival and subsequent population impacts. To our knowledge, this is the first known case of infectious disease leading to increased early reproduction in a mammal.

It's a simple response: young breeders used to have lower fitness, because of competition from older adults. Now, the high mortality after the first year has made it a losing strategy to wait to reproduce. When the early breeders are the only ones having many offspring, the population will evolve quickly to early breeding.

References:

Jones ME, Cockburn A, Hamede R, Hawkins C, Hesterman H, Lachish S, Mann D, McCallum H, Pemberton D. 2008. Life-history change in disease-ravaged Tasmanian devil populations. Proc Nat Acad Sci USA (in press) doi:10.1073/pnas.0711236105

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

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 75–85% 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 (3–7% 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 “typical” 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

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)

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

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

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

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 was surprisingly little response from other nearby elephants. Older calves were attacked and killed within 50 m of the drinking bulls. The distress calls of the young elephant and lion growls seldom distracted them from drinking.

Tough to be a young male elephant.

References:

Joubert D. 2006. Hunting behaviour of lions (Panthera leo) on elephants (Loxodonta africana) in the Chobe National Park, Botswana. Afr J Ecol 44:279-281. DOI

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

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!

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.

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.

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

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

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

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.