phylogeny

I ran across this paper from a few years ago by John Avise and DeEtte Walker, which considers the implication of reticulation-based species concepts for mtDNA-generated phylogenies.

After quoting Dobzhansky on natural categories, they point to the central problem with using mtDNA phylogenies to define species: a clonally inherited gene does not easily lend itself to testing horizontal gene transfer:

In this same spirit, we ask here whether biotic discontinuities as seen through the eyes of laboratory-based mitochondrial geneticists tend to bear resemblance in number and composition to the biological units currently recognized as taxonomic species. There are additional reasons for interest in the outcome. First, discontinuities might be evident in local biotas (the nondimensional species perception) but may blur when geographic variation is taken into account. Molecular phylogeographic studies address this issue, because they explicitly analyze spatial variation (6, 7). Second, under the biological species concept (BSC), a sexual species usually is perceived as a reproductive community whose gene pool retains coherency primarily via the bonds of interbreeding and genetic exchange (1, 8); however, mtDNA molecules are transmitted asexually, and matrilines are nonreticulate. Thus, any genuine unities within (and discontinuities between) groups of organisms in mtDNA genotype cannot be attributed to "horizontal" patterns of contemporary lineage anastomosis via mating per se. Instead, they must be caused by "vertical" connections (and partitions) in matrilineal phylogenies. However, vertical connections themselves are functions of the demographic histories of population units demarcated by temporally extended patterns of interbreeding and gene flow.

I think this passage puts the situation more direly than deserved -- after all, every gene is vertically inherited. Mitochondrial DNA is no exception. It can be transferred by gene flow just as surely as any autosomal gene.

No, the key difference is that clonal inheritance leaves mtDNA with a greatly reduced effective size compared to autosomal (or X-linked) genes. This means that a given amount of gene flow is vastly less effective at dispersing mtDNA variants. Hence mtDNA (and Y chromosomes) have much higher F_ST (at equilibrium) than other genetic markers.

In other words, longstanding populations within a species will tend to look more divergent considering only their mitochondrial DNA than considering their autosomal genes. We can see this pattern when considering differences among subspecies of chimpanzees and other hominoids. The subspecies are highly distinct from each other considering only their mtDNA, with long divergence times ranging higher than a million years. The other uniparentally inherited genetic system, the nonrecombining portion of the Y chromosome (NRY) shows a similar pattern -- subspecies of chimpanzees are highly distinct, sharing no NRY lineages (Stone et al. 2001). In contrast, there is substantially more sharing of variants at autosomal sites (Fischer et al. 2004). Chimpanzee subspecies share many fewer autosomal variants than are shared among human groups, but they share many more autosomal than mtDNA or Y chromosome variants. Gorilla genes follow a similar pattern: mtDNA indicates very strong divergence between western and eastern gorillas, while autosomal genes show evidence for recurrent gene flow between them up to 150,000 years ago (Thalmann et al. 2007).
Avise and Walker compared mtDNA phylogenies for vertebrates with commonly accepted taxonomic species, finding roughly twice as many deep mtDNA phylogroups as taxonomic species. They consider that these generally represent historical patterns of demography and constrained gene flow within species.

Coalescent patterns in gene trees are related intimately to historical patterns in population demography (7, 21, 22). In particular, tight connections among nonanastomose [nonreticulating] genotypes suggest recent lineage coalescence to a shared ancestor, likely because of relatively small evolutionary effective population sizes that cause extant lineages to have shallow temporal depth. Conversely, large genetic gaps between gene-tree branches suggest long-standing historical population separations. In support of this likelihood, nearly all of the deep phylogenetic disjunctions registered in the intraspecific mtDNA gene trees in this review involved regionally separate populations.

This is basically saying that regional differentiation within species is an important source of genetic variability. They mention that male-mediated dispersal would create patterns not easily tested with mtDNA; this is one factor but broadly, any single gene will create a phylogeny that is potentially discordant with others in various ways.

References:

Avise JC, Walker D. 1999. Species realities and numbers in sexual vertebrates: Perspectives from an asexually transmitted genome. Proc Nat Acad Sci USA 96:992-995. Abstract

Fischer A, Wiebe V, Pääbo S, Przeworski M. 2004. Evidence for a complex demographic history of chimpanzees. Mol Biol Evol 21:799-808. doi:10.1093/molbev/msh083

Stone AC, Griffiths RC, Zegura SL, Hammer MF. 2002. High levels of Y-chromosome nucleotide diversity in the genus Pan. Proc Nat Acad Sci USA 99:43-48. doi:10.1073/pnas.012364999

Thalmann O, Fischer A, Lankester F, Pääbo S, Vigilant L. 2007. The complex evolutionary history of gorillas: insights from genomic data. Mol Biol Evol 24:146-158. doi:10.1093/molbev/msl160

The April issue of Discover has a feature article on PhyloCode, focusing on the roles of Jacques Gauthier and Kevin de Queiroz in trying to revise the code of biological nomenclature. It is an interesting introduction to the issues, but is a little short on specifics, so I went to some additional resources to examine the impact of the whole PhyloCode debate on human phylogenetics.

Proliferating ranks

PhyloCode is an attempt to address two simple problems with the Linnaean system. The first is the problem of ranks. The Linnaean system provides seven ranked positions for species and higher-order taxa. These are the levels familiar to anyone who can remember King Phillip's soup, or his Peter's German origin, or any of the other mnemonics. These seven levels (kingdom, phylum, class, order, family, genus, species) have been supplemented over the years with in-between levels at almost every rank, such as suborders and infraclasses. For example, the most basic division among living primates is into superfamilies, which is the rank occupied by hominoids (great apes and humans), cercopithecoids (Old World monkeys) and ceboids (New World monkeys). The grouping of all three of these superfamilies, Anthropoidea, is a suborder, while the grouping of Old World monkeys and hominoids is the infraorder Catarrhini.

But when it gets to the level of infraorders and superfamilies, the phylogenetic pattern of relationships is already stretching the Linnaean classification to its limits. This degree of differentiation is more or less well suited to primates, but many other groups of organisms have even more complicated phylogenies with many more branches. This leads to some big confusion:

As part of their work, [Gauthier and de Queiroz] created a lizard family tree, but when they began to assign names to the important branching points on the tree, they realized there were more groups to name than there were ranks in the traditional system. "I started using these exotic ranks like parvorder, cohort, and microorder, and all that kind of crap," Gauthier says. "Then we'd learn more about the tree, and all the names would have to change. I thought, 'That sucks. All these ranks, they're a problem.'" (Foer 2005:48-49)

This is a problem I've thought about for a while also, ever since I was learning Mesozoic mammals and encountered exotic taxonomic ranks like "tribe" and "domain." Unlike suborder and infraorder, many of these give no indication at all about where they belong in the phylogenetic hierarchy. If this complication actually helped organize species, that would be forgivable. But even the extension to thirty or more ranks is not enough to encompass all the possible groupings in some phylogenies, especially where extinct species must be placed in a hierarchy including living species and their ancestors.

And of course the probability of disagreement among authorities on names increases combinatorially with more taxonomic ranks. Even within the hominoids there is at present substantial disagreement on the names of groups at almost every taxonomic level, despite the fact that almost everyone agrees about the phylogeny of the living species of apes and humans. Some of this disagreement is purely nomenclatural, while the rest comes from genuine disagreements about the phylogeny of extinct apes. It seems especially problematic that disputes about the relationships of extinct and fragmentary fossils could substantially alter our judgment about the nomenclature to apply to living species, but that is exactly where we stand.

Hominids and hominins

This leads to the second major problem of the Linnaean system, the problem that the names of groups themselves are formulated in a way that cannot be divorced from their taxonomic level. What this means is that if our hypothesis of phylogeny changes, the names of taxa must also change. The problem with this is that it subverts the goal of communication:

In the zoological code, family names must end with the four letters idae, for example, and subfamily names must end in inae. If taxonomists decide that a group once considered a family should instead be ranked as a subfamily, the group must, under the rules of the current system, get a new name. This frustrates the PhyloCoders to no end. "It's still the same tree," Gauthier says. "Nothing has changed, except how we spell the names. In a day when all this information is going onto the Internet, this is a bad idea. It's a constant change of PIN numbers." Some taxa have gone through a number of different names over the course of just a decade. Several years ago, for instance, it was decided that the great-ape family Pongidae couldn't exist at the same rank as the human family Hominidae because humans are a subset of the great apes. To fix the problem, researchers proposed that humans and their great-ape relatives be combined into a single family, Hominidae, and members fo the family Pongidae became the subfamily Ponginae. This can make literature searches a real pain, Gauthier says: "To a computer, there is a world of difference between iguanidae and iguaninae" (Foer 2005:50).

In my mind, computers are the least of the problem. Replace "to a computer" with "to an undergraduate" and you are closer. Really, even this understates the problem. If we could ensure that a new taxonomy established by universal consensus today would not change in the future, then it would be well worth changing all the names. But we can be pretty sure that things will change in the future, repeatedly. It just isn't worth having a system where the names have to be changed all the time, because such changes render all past research at best confusing, or at worst nonsensical.

The Hominidae-Homininae problem is not the only one in paleoanthropology, but it is a convenient example. Foer's description of the problem is one possible reformulation, but not the most popular one. We all recognize that African apes and humans are more closely related than either is to orangutans, and chimpanzees and humans closer than either is to gorillas. Many people would apply Hominidae to all the great apes, ponginae to orangutans, and homininae to the African apes and humans. This leaves the human lineage (including australopithecines) in the "tribe" Hominini (The tribe Panini would therefore include tasty Italian bushmeat sandwiches). Thus, orangutans would be hominids, gorillas would be hominines, and australopithecines would be hominins.

Consider the problems with this arrangement. First, it isn't comprehensive. There is no name for the human-chimpanzee clade, for example. The taxonomic level for that clade would properly depend on the details of the evolutionary divergence among gorillas, chimpanzees, and humans. If, for instance, there was a substantial adaptive radiation between the gorilla divergence and the human-chimpanzee divergence, then these fossil lineages might be placed with chimpanzees and humans within an infrafamily, with the chimpanzee-human clade placed as a supertribe. Likewise, the branch points leading to the dryopithecines depend on their relationships with the later African apes, or even to the Asian apes. In other words, the taxonomy still hangs on currently unknown phylogenetic branchings, and the choice of taxonomic level is entirely arbitrary.

The arbitrariness of the naming system is highlighted by some other alternatives for the hominoids. For many years, molecular researchers like Morris Goodman have suggested that the genetic similarities between chimpanzees and humans are consistent with those within genera of most mammals, and the time of origin of these lineages is also consistent with the antiquity of mammalian genera. So Goodman et al. (1998) took the logical step of including both humans and chimpanzees in Homo. The great apes in this scheme are all hominins (tribe Hominini) and the living hominoids are all hominines (subfamily Homininae).

By discarding past consensus, arbitrary changes impose a cost on any researcher or student, in discarding past consensus. The past fifty years or more of paleoanthropological research have shared a clear meaning for the term "hominid." Of course, one may read that literature today while remembering the past meaning of "hominid," just as we remember what "pithecanthropine" used to mean. But it is a cost that should come at some benefit. For "pithecanthropine," the loss of the genus Pithecanthropus combined with the discarding of the idea of a "pithecanthropine stage" of human evolution means that we no longer have any call to use the term. The benefit of the change is simplification and the recognition that an incorrect hypothesis of evolution has been refuted.

Many would argue that the replacement of hominid with hominin has similar benefits. After all, the use of "hominid" in the past was partly conditional on the acceptance of the family Pongidae to hold the great apes. Now that we know that humans and African apes are sister taxa, we should construe Hominidae differently. It is clear that the human lineage did not have a long independent evolution during the Miocene, that its origin is comparatively recent compared to other mammalian families, and that the gross genetic distinctiveness of humans is relatively low. Doesn't it therefore clarify our understanding of hominoid evolution to demote the human lineage from a family-level taxon to a lower taxonomic level?

The clade formerly known as Hominidae

The problem with this line of logic is that it is a purely aesthetic choice. There is no reason to suppose that a family-level taxon should have a particular date of origin or duration. One may argue that extant mammalian families have a distribution of ages, or even of genetic variation, and that this should inform our taxonomic choices. But the logical endpoint of this argument is not that the human lineage is a tribe-level or infrafamily-level taxon, but instead the endpoint is the conclusion of Goodman et al. (1998), that the human lineage is a subgenus-level entity and chimpanzees should be placed in Homo. The fact that this solution is viewed as "too extreme" is good evidence that this is at its core an aesthetic concern rather than a scientific one.

In fact, there is no scientific reason why a particular phylogeny should correspond to a particular range of phylogenetic ranks. Many extant families of organisms include hundreds of species, others include only one. Some extant vertebrate families originated in the Paleozoic, others in the Pliocene. And viewing only the variation of extant species is especially misleading on this issue. When we consider the relationships of extinct organisms, we find family-level groups originating across the history of the earth. The family rank has been applied to short-lived groups with uncertain affinities, to extinct collaterals of living orders or classes, and to single fossils. When it has been applied, it has usually been according to considerations of morphological adaptive pattern. On this basis, there is a good argument for the idea that the human lineage should be at the family rank, regardless of its antiquity. The adaptation to an obligate pattern of bipedalism along with the dental specializations of the australopithecines (shared with humans) set them apart from other apes to a greater extent than any great ape. These features probably mark the human lineage as substantially different from great apes in adaptive terms as the great apes are from hylobatids.

So what aesthetic considerations prevent us from simply continuing to calll the human lineage Hominidae? That usage requires that something be done to avoid a paraphyletic taxon including orangutans, chimpanzees, and gorillas. We seemingly have a choice: accept Gorillaidae, Panidae, and Pongidae alongside Hominidae, or demote all these taxa. The demotion also helps with (although does not solve, see above) the problem of assigning taxonomic ranks to the African-European ape clades. A lower-level human clade leaves more ranks below superfamily to apply to the great ape clade, its possible progenitors among the Afropithecinae or Proconsulidae, the possible ancestors of the African ape clade among the Dryopithecinae, and the possible ancestors of the human-chimpanzee clade. Each of these clades may need a rank, and there aren't enough ranks to go around.

I have no problem with aesthetic changes in nomenclature per se. After all, I wholeheartedly support replacing "Neanderthal" with "Neandertal." And in fact, I don't find "hominin" that objectionable. It may take me a while to get used to the sound of it, but it is very clear in its now-current application. Since it merely replaces the old use of "hominid," it is a simple replacement of one unambiguous term for another. It seems to me much better than relegating the human lineage to a subgenus, which would leave no taxonomic names at all to talk about the origins of the human lineage (notice how much more awkward this becomes when we can't say "hominid origins").

What I don't like is the confusion that comes from changing the meaning of "hominid." "Hominin" means nothing special to anyone now, so it has a low conceptual cost. In contrast, "hominid" until recently meant something entirely different from its proposed meaning, inclusive of all great apes. "Hominid" is how countless interested followers of paleoanthropology recognize our ancestors, and it is how many of us have presented our science publicly throughout our careers. It is bad enough that we have to get our students to understand that "hominoids" are not "humanoids," and "hominids" do not include all "hominoids." Now we have to get them to differentiate "hominins" from the rest.

An argument is that "hominin" is qualitatively more valuable than "hominid," because it conveys a more correct view of the human phylogenetic rank in comparison to other groups of mammals. This would be the "Copernican" analogy -- noting that the sun is the center of the universe "puts humans in their place," and noting that our taxonomic level is at the tribe rather than the family likewise shows how our place is less special among the species of the natural world. Or at least, it does not distort our view of ourselves by giving us a higher taxonomic rank than we deserve.

But of course, if it is our goal to have every name indicate its exact rank relative to other organisms, then we must also make mammalian groups consistent with insect groups, mollusc groups, and plants, for that matter. For this purpose, it might be as well to include a number after every taxonomic name, to represent the genetic variation encompassed by the group, or age of the group in millions of years, for example.

And more to the point, the next time someone decides that the hominoids subsume too small a segment of the mammalian phylogeny, it will seem necessary to some revolutionaries to change the taxonomy yet again. When we revise terms to give a "correct" understanding of their status, there is no end to "corrections" in pursuit of this goal.

So there are good reasons to resist the shift to "hominin." It renders "hominid" inconsistent with its historical usage in the literature. It unnecessarily confuses the public, especially those who follow our science at a distance. And most important, there is no guarantee that this change will be the last.

How does PhyloCode help?

This is not a full summary of the rules of the PhyloCode. These are available online.

PhyloCode is a system for naming clades. Under this system, each clade in the phylogenetic tree of life is eligible for a unique name. These names are not ranked, so that although clades are necessarily hierarchical, their names are not systematized in a hierarchical way. There are two basic reasons for the use of rankless names:

1. The number of clades on some phylogenies is so extensive that a rank-based classificaiton devolves into confusion.
2. Under a rank-based classification, any change in the rank of a single clade name requires concomitant changes to many other clade names, although neither their content nor their hierarchical placement has changed.

Thus, the PhyloCode "holds clades innocent" of changes in other clades, by retaining a single, unique, unchanging name for them.

Clades are may be defined in a number of ways, including by apomorphies, by descendants of a single ancestor, or by the inclusion of all species joined by a single node. This last, node-based clade definition is probably the most common. For example, the living African apes and humans belong to a clade that we might call "Clade Homo sapiens and Gorilla gorilla", while humans and australopithecines may be joined in "Clade Homo sapiens not Pan troglodytes."

Part of the appeal of this kind of scheme is that it approximates what we do much of the time anyway. The human-chimpanzee clade has no taxonomic name, at least not that most people would know, and when we talk about it, we use the term "human-chimpanzee clade." It is understood that this clade also includes Pan paniscus, and that bonobos are nevertheless not part of the name, although "human-bonobo clade" would be no less correct. For larger taxonomic groupings, this trends toward a kind of shorthand. "Human-gorilla" clade necessarily includes chimpanzees and bonobos, and it shorter than "the clade containing extant African apes and humans." PhyloCode effectively codifies this shorthand.

But at the same time it provides a procedure for giving each of these clades a name. Remembering that these clade names carry no rank information, it is possible to give every one of these clades a name that is at once unique and resistant to change with changes in our understanding of phylogeny within and outside of the hominoids.

Phylocode and hominoids

Considering all this, one may wonder what the PhyloCode proposal would say about our current taxonomic problems in paleoanthropology. In the central instance, does PhyloCode provide a way out of the hominid-hominin problem?

According to the current draft (June 2004) of the PhyloCode, "phylogenetic definitions for many widely used clade names" (Cantino and de Queiroz 2004:4) will be presented in a volume resulting from the first meeting of the International Society for Phylogenetic Nomenclature, in Paris, July 2004. That volume is not yet available, but the abstracts of the meeting have been compiled and are available in
a PDF online.

Representing primate systematics at the meeting was a contribution from Kaila Folinsbee and David Begun. The part pertaining to Hominidae reads as follows:

We propose to redefine Hominidae Gray 1821 (converted clade name) as the most inclusive clade containing Homo sapiens and Pongo pygmaeus. We redefine Homininae Gray 1825 (converted clade name) as the most inclusive clade containing Homo sapiens and Gorilla gorilla not Pongo pygmaeus. Hominini Gray 1825 (converted clade name) includes Homo sapiens but not Pan troglodytes. The Ponginae has traditionally been paraphyletic, separating Pongo pygmaeus, Gorilla gorilla and Pan troglodytes to the exclusion of Homo sapiens. Ponginae Elliot 1913 (converted clade name) is defined as Pongo pygmaeus but not Homo sapiens. These converted clade names preserve the established endings of the older system in order of most to least inclusive. (Folinsbee and Begun 2004:39)

In other words, this enshrines the use of "hominin" for the human lineage and "hominid" for the great apes and humans.

I think this is unfortunate, since the opportunity was there to establish a classification that would be at the same time unambiguous and maximally consistent with historic use of the term "hominid." To do so, a different term for the great ape and human clade would have to be invented or drawn from the literature. But the strength of the PhyloCode is that this name would not have to be at a higher rank than Hominidae. So for example, all the great apes and humans could be classified in Pongidae, with the human lineage assigned to Hominidae. Retaining "hominid" for the human clade would have followed the PhyloCode recommendation for converting clade names under the old system to the new one:

Recommendation 10A. Clade names should be selected in such a way as to minimize disruption of current and/or historical usage (with regard to composition, diagnostic characters, or both) and to maximize access to the literature. Therefore, when establishing the name of a clade, a preexisting name that has been applied to that clade, or to a paraphyletic group stemming from the same ancestor, should generally be selected if such a name exists. If more than one preexisting name has been applied to the clade (including those applied to paraphyletic groups stemming from the same ancestor), the name that is most widely and consistently used for it should generally be chosen (Cantino and de Queiroz 2004:26).

Under this recommendation, the wholesale switch from "hominid" to "hominin" would not be the preferred outcome. Nevertheless, the case for resisting the classification as proposed is weak, and likely futile.

The most important consequence of the PhyloCode may be in strengthening the hand of conservatives in the future. The classification of the hominoids has for the past few decades been characterized by a pressure to place the human lineage at a lower and lower taxonomic rank. This revision began with Ernst Mayr, has continued through the elevation of "Hominidae" to include all the great apes, and is expressed today by geneticists who would like to include chimpanzees in Homo. This trend has had the primary motivation of making the hominoid taxonomy "equivalent" to that of other vertebrate taxa, with a secondary, often unstated, goal of demoting the status of humans in the natural order. There is every reason to suppose that both these motivations will continue in the future.

But the PhyloCode classification helps make it possible to retain the same names even in the As proposed, the PhyloCode recognizes the names "Hominidae," "Hominini," and others as rankless clade names. Thie means that even if the classification changes substantially in other ways (for example, placing chimpanzees in Homo), we still can use these rankless names for the clades in the hominoid phylogeny. The human lineage can be "Hominini" whether it is technically equivalent to an old-style subfamily, tribe, or subgenus, in other words. But more importantly, if rankless names are recognized widely among the mammals, then there is less of a reason to require clade names to be made consistent across the mammals. Instead, we can move to a direct reference to the age of clades, or the level of genetic differentiation they represent, or other quantitative considerations. This would be a step forward in phylogenetic classification.

Names of fossil hominid genera

Although the phylogeny of the extant hominoids is well understood, the phylogeny of fossil hominids (or hominins) is not. There are several outstanding problems, including whether the robust australopithecines are monophyletic, the relationships of the habilines, and more minor problems such as the placement of Sahelanthropus, Kenyanthropus, and Ardipithecus relative to other fossils and (arguably) extant hominoids. For these problems, PhyloCode provides some assistance.

Most important is the option to define clade names conditionally upon the acceptance of a particular phylogeny:

11.9. In order to restrict the application of a name with respect to clade composition (i.e., under alternative hypotheses of relationship), phylogenetic definitions may include qualifying clauses specifying conditions under which the name cannot be applied to any clade (see Example 1). It is also possible to restrict clade composition under alternative hypotheses of relationship through careful wording of definitions (see Examples 2 and 3) (Cantino and de Queiroz 2004:29).

This is clearly useful for the hominid phylogeny. For example, a careful definition might classify the robust australopithecines as a clade including both A. boisei and A. robustus. The node connecting these two species might well also include the species A. aethiopicus, or it might not. A definition conditioned on the inclusion of that species would encompass those phylogenetic hypotheses in which these three species are monophyletic. Such a clade might simply be named Paranthropus, or it might be desirable to give another taxonomic designation, such as "Paranthropina." The process explored by this example could easily be extended to other cases.

A question is whether this all goes too far toward the cladistic extreme of classification. There are a number of nontaxonomic names now applied to the hominids, including "australopithecine," "habiline," "human," "Neandertal," and others. Under Simpson's classification, these would be called N₂ names, and their strength is precisely that they are not taxonomic. The extension of any one of them can change according to convenience, and is not necessarily constrained by considerations such as monophyly.

There is certainly a utility to continuing to use nontaxonomic names like these, as long as adaptation is part of our consideration of evolutionary history. It is almost certainly true that humans derive ultimately from some species of australopithecine. But that does not mean that we should not talk about australopithecines, just as a definition of Dinosauria that includes birds does not mean that we should stop talking about dinosaurs.

Conclusions:

I started writing this essay while deeply considering a problem: is it time to switch to using "hominin?" This is more or less urgent to me because I have a textbook for which a decision must be made. It is not too late to search-and-replace "hominid" throughout. I have no special reason to use "hominin" myself; indeed I find it distasteful to do so. I like "hominid" -- it's the way I learned the field. And I happen to think that our adaptive differences from other primates deserve a high-rank designation, regardless of our genetic similarities.

Yet, "hominin" has a formidable position. It has swept beyond a small clique of scientists to encompass most of the new announcements of species in the field. Those most conversant in taxonomy are not the most prolific in terms of publications, but everyone who names anything must have a full understanding of these issues, and in this realm, the assault of "hominin" has been unrelenting. And within the last year popular publications have begun to regularly use "hominin." For example, National Geographic uses the term in two articles in their April 2005 issue, postfacing it as "a term for humans and their relatives."

The use of the term is no longer just an option, it is approaching the default. The PhyloCode is far from acceptance among taxonomists, but by providing a rank-free naming system for clades, it created the potential to avoid the issue. Except that the founding conference of the system introduced as an integral element the nomenclature applying "hominin" to the human clade and "hominid" to the great ape clade. So all escape routes appear to be blocked. There is only the unrelenting attrition imposed by the taxonomic cognoscenti.

All this means that if I continue to use the term "hominid," I should have a principled reason I am willing to stand by. And I don't. Nostalgia is not a principle. I myself am not confused by older literature that uses "hominid," and I am not convinced that my students will be confused, either. For undergraduates, it's just another name to learn. And if popular magazines are blithely using the term, the public is just going to have to follow. In the end, I think there will be a cost, borne by all of us, but hopefully the change will be more or less permanent and any hard feelings soon forgotten.

So sometime fairly soon, I will probably resign myself to saying "hominin," and using only my right hand on the keyboard instead of both. And maybe I'll take the edge off by writing some taxonomy myself. Any suggestions for clade names are welcome.

Afterword: Where did hominin come from?

I have never seen a review of where the usage of "hominin" came from, and how it became common in paleoanthropology. A search of journals indexed by ISI finds the first keyword reference to "hominin evolution" in a 1993 paper on Makapansgat paleoenvironment in JHE by R. J. Rayner, B. P. Moon, and J. C. Masters. The most widespread early use of the term appears to have been by Bernard Wood and his collaborators. I have not done a systematic review, if anyone has any insight on this I would be most pleased to hear of it.

References:

Cantino PD and de Queiroz K. 2004. PhyloCode: A Phylogenetic Code of Biological Nomenclature. PDF available online

Foer J. 2005. Pushing PhyloCode. Discover 26(4):47-51.

Folinsbee KE and Begun DR. 2004. Phylogenetic nomenclature of living and fossil catarrhines. In First International Phylogenetic Nomenclature Meeting Abstracts, M Laurin, ed. p. 39.
PDF available online

Goodman M, Porter CA, Czelusniak J, Page SL, Schneider H, Shoshani J, Gunnell G, Groves CP. 1998. Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol. 9(3):585-598.
PubMed

Rayner RJ, Moon BP, and Masters JC. 1993. The Makapansgat australopithecine environment. J Hum Evol 24(3):219-231.

Speciation is the cessation of interbreeding between one animal population and all other populations with which it formerly exchanged genes. When interbreeding between two populations is interrupted, they will become genetically differentiated because the force of gene flow can no longer maintain their similarity. The other evolutionary forces then combine to make the populations diverge:

1. Genetic drift causes each population to lose alleles. Because drift is a random process, it is likely that each population will lose different alleles, making them steadily more different.
2. Natural selection will cause the populations to adapt to their environments. When these environments are different, the adaptations of the populations will be different as well.
3. Unique mutations that occur in individuals in each population cannot move to the other, and as these mutations grow in number, the populations become more genetically different.

If interbreeding is not restored between the populations, the accumulated amount of genetic and phenotypic changes between them eventually will make interbreeding impossible. When one population ceases to interbreed with all other populations, its evolutionary history diverges because genetic changes cannot cross the reproductive barrier. Simply put, the population resulting from a speciation is a species.

Patterns of speciation

Reproductive isolation can occur because populations become physically separated from each other. In primate evolutionary history, this scenario has occurred many times, for example, when anthropoid monkeys first arrived in South America some 50 million years ago. At that time, South America was an island continent separated by ocean from both North America, with which it is presently connected, and Africa, with which it had been connected before about 80 million years ago. The leading hypothesis for this original dispersal of monkeys to South America is that a small number of individuals crossed the then-smaller South Atlantic Ocean on storm-swept "rafts" of logs and other vegetation. Such a dispersal may have depended on the presence of volcanic islands between the continents which no longer exist, or patterns of ocean currents that were stronger when the two continents were closer together (Flynn and Wyss 1998). Like primates, rodents also apparently reached South America by this mechanism. However, the survival of such colonists and their establishment on the South American shore was a rare, unlikely event, and upon their arrival these early anthropoids were stranded with a formidable isolating barrier, the Atlantic Ocean, preventing subsequent mate exchange with their African relatives. Many similar colonizations, usually less spectacular in scope, have occurred throughout primate evolution, including dispersals at different times from Asia to Africa, Africa to Eurasia, and North America to Eurasia.

Populations need not cross oceans or move among continents to become isolated from each other. Isolating barriers may arise for many reasons, including when high water levels separate islands from the mainland, when a drier climate spreads grasslands and divides areas of forest, and when an area in the midst of a population's range undergoes geologic uplift, forming hills or mountains. Isolation caused by physical separation between populations leads to allopatric speciation, meaning that the populations live in different geographic areas from each other.

Peripatric speciation, on the other hand, occurs between populations that are not physically isolated from each other. A large population may be spread across a wide range of local environments that slightly differ from each other. On the edge of such a range, small local groups may be strongly affected by natural selection, tending to adapt them to their distinct environments. If survival at the edge of the range is difficult, such groups may not persist for very long, or may be mostly composed of migrants from the main population from the center. Such a population structure leads to the "center-and-edge effect," in which variation is greater at the center of the species range and limited by genetic drift at the peripheries of the range.

But if new adaptations in the edge subpopulations allow them to survive and proliferate, and the amount of gene flow from the rest of the population is small, then the force of natural selection may overcome the tendency of gene flow to limit divergence. As a subpopulation at the edge of the range becomes more adapted to its local conditions, reproductive contacts with the rest of the population may become less important. Individuals with genes from the center may be at a selective disadvantage, or reproductive contact may be lost entirely. This process can result in speciation, if the edge subpopulation succeeds.

Allopatric vs. peripatric speciation

Reproductive isolation

The process of speciation involves an interplay of all the evolutionary forces that affect populations. The key factor is the cessation of gene flow between the populations involved. Speciation requires more than simply isolation, however. If two subpopulations once separated by geography are brought back into contact, without any other evolutionary changes to impose continued reproductive isolation, they will resume interbreeding with each other. In such a case, no speciation has occurred.

Such circumstances have continually happened to human populations. Often when a human population colonizes a new area, it becomes isolated from other populations for a period of time, sometimes hundreds of generations or more. For example, the initial colonization of the Americas across the Bering land bridge, at least 12,000 years ago, was followed by the isolation of peoples on these continents from the rest of the world after the post-glacial rise in sea levels cut off any further land access. But when the invention of ocean travel reestablished transoceanic contact, people resumed interbreeding, as attested by the large numbers of their common descendants today. This kind of isolation affected other areas, including Australia, where only intermittent immigration from Southeast Asia occurred after the initial habitation of the continent over 50,000 years ago. Even over such long periods of time, these populations experienced no changes in their reproductive functions, and therefore no speciation occurred.

Isolation is initiated by a physical fact: the loss of gene flow between populations. But it is made permanent by the subsequent evolution of reproductive functions in one or both populations. Such reproductive changes occur either (1) as a side effect of adaptive changes in other biological aspects of the population or (2) as part of a process of continual reproductive change that causes populations to diverge after physical or geographic isolation is established.

Processes of continual reproductive change are expressions of sexual selection. In many groups of animals, mating involves a complicated interplay of physical traits and behaviors that animals use to advertise their qualities to potential mates. In every group, the ability of an animal to recognize potential mates depends on the presence of these signals, called the "mate recognition system". In some groups, the mate recognition system depends on the presence and form of specialized anatomical features, such as the antlers of elk or the special facial coloration of mandrills. In other groups, an animal must perform special behaviors for mate recognition to occur. Like any other phenotypic characteristic, these features may evolve over time, either because of changes in the selective balance between these reproductive features and other features leading to reproductive success or because new behaviors become associated with mate desirability. Many of the more complex mating behaviors may be mostly transmitted by learning or observation, only weakly heritable, allowing mate recognition systems to change easily over short periods of time. Two populations that lose genetic contact will be very unlikely to evolve in the same way. If separated for any period of time, members of one population will not recognize the members of the other as potential mates, resulting in speciation.

The ability to reproduce may also be lost for other reasons. Many times, evolutionary change in chromosomal structure or genetic function may occur that makes reproduction impossible even if mating occurs between members of two populations. The chromosomal rearrangement during human evolution that gave us 46 chromosomes instead of the 48 in chimpanzees would by itself make chimpanzee-human hybrids impossible. In other cases, mating and the birth of hybrid offspring between two populations may occur, but genetic changes may make these offspring sterile. This is the case for horses and donkeys, which interbreed with each other, but produce sterile mules as offspring.

Speciation as a hypothesis

It is important to bear in mind that speciation is a concept that must be tested as a hypothesis of population relationships. In particular, when biologists say that a speciation has occurred, they hold the hypothesis that the resulting populations will never again exchange genes in a way that significantly shapes their evolution. The hypothesis of speciation can be tested only by the presence of absence of gene flow.

Often, reproductive isolation is maintained primarily by the continued geographic isolation of the populations involved, even if other substantial evolutionary changes have occurred. Prominent examples are found among zoo animals. Sometimes animals that never have the opportunity to encounter each other in nature are found to interbreed freely when placed in close proximity to each other in zoos. For example, common chimpanzees and bonobos are separated by geographic barriers in the wild: bonobos live only south of the Congo River and common chimps only to the north. These two groups practice distinctive mating behaviors and have some anatomical differences. However, when given the opportunity in captivity, they do interbreed and produce hybrid offspring. Likewise, Sumatran and Bornean orangutans are presently isolated in the wild, and their genetic differences indicate that gene flow between the populations was very limited or nonexistent even during periods when these islands were connected to each other, either because their forested habitat did not extend across the now-submerged land bridge or because intermediate populations died out (Warren et al. 2001). However, there are only slight apparent anatomical differences between the two populations, and they interbreed quite freely in captivity.

In these instances, it is not obvious whether speciation can be said to have occurred. Clearly the populations involved have been geographically separate for a long time, with no immediate prospect of rejoining each other in their natural ranges. If they were to contact each other in the wild, it is impossible to predict whether gene flow would be reestablished. Future events may or may not reestablish gene flow, so that neither the hypothesis of speciation nor the alternative hypothesis of no speciation can be refuted. Both hypotheses are untestable, because we cannot foretell the future relationships among these organisms.

Sometimes nature permits stronger tests, even when interfertility is possible. For example, lions and tigers are closely related to each other and occurred historically in overlapping geographic ranges in Asia. While the skeletal differences between them are slight, these two kinds of great cats obviously differ in coloration and external anatomy, and in the wild they are successful only in different environments. Tigers are adapted to hunting in densely vegetated areas and lions are adapted to grassy plains. In captivity these two cats can and do produce fertile offspring, called "ligers" or "tigons" (More on hybrid big cats). Even so, apparently mate recognition between these cats does not occur in the wild, even if they are in close contact, which by itself would tend to support the hypothesis of speciation between them. However, a speciation between the two forms is further supported by their reactions to habitat changes that have occurred in their Asian ranges. Lions and tigers remain limited to their environments of greatest adaptation, without moving into each other's ranges, and even under habitat pressure and reduced numbers they do not seek out each other as mates. Thus, gene flow will play no part in their future, even if their human managers allowed it.

In some other cases gene flow extends across a considerable range but does not connect one end of the range to another. It sometimes happens in nature that a long string of interbreeding populations all exchange mates with their immediate neighbors but not over long distances. Genes may flow across the entire length of the chain by continued exchange from one population to the next, and by this mechanism mutation, selection, and genetic drift may cause changes in the entire population. However, when individuals from either end of the chain are brought together, they may be intersterile. Such populations are sometimes called "ring species", especially when they occur around the edge of a large isolating barrier, such as a body of water. Such instances may be difficult to resolve with the concept of speciation, although any large population may contain pairs of individuals who cannot reproduce with each other, but might each reproduce with others. In the case of ring species, speciation may follow quickly if any of the intervening populations lose genetic contact.

Speciation and evolution

The branching process that describes how different kinds of organisms arise is at a different level than the reproduction of organisms within a population. Each speciation is the birth of a new species, and species may disappear by extinction, when none of their members survive. Speciations and extinctions follow a different pattern than the births and deaths of individuals within a population, and although both speciations and extinctions are the result of evolution within populations, their pattern cannot necessarily be predicted from the forces of evolution alone. The study of the factors influencing speciation, extinction, and the resultant diversification of different species of organisms is called macroevolution, while the regular forces of evolution within populations are often called microevolution in contrast.

Macroevolutionary and microevolutionary patterns can reinforce each other during speciation. The initial speciation of a new species may accompanied by strong selection to a new environment. One change may trigger others, and the species may rapidly change in many respects. New anatomical configurations may evolve, along with new behaviors that define a new adaptation with respect to other species in the environment. The new advantages of this species may allow it to spread beyond the range of its parent species, or it may spread back into the parent's range, replacing it. Such broad evolutionary changes might have been impossible without the action of selection and drift in the small isolated population created by speciation.

Because of this possibility of great evolutionary change at the time of speciation, some scientists believe that most evolutionary change happens during these events, and not at other times. This hypothesis is most notably expressed by the model of punctuated equilibrium proposed by paleontologists Niles Eldredge and Stephen Jay Gould (1972). This model predicts that most populations stay mostly the same for long periods of time, a state called evolutionary stasis. Only occasionally, driven by environmental events, do large populations sizes with selective optimizations in a particular environmental niche break down, resulting in the rapid adaptation of small populations to new adaptive niches and new combinations of genetic material. Thus, in punctuated equilibrium, evolution consists of long periods of stasis interrupted by bursts of change that include speciations.

This model may explain the fossil records of different animals that remained relatively unchanged for long periods and then changed greatly in a short time. For example, . Such examples might involve speciations and subsequent rapid adaptations. On the other hand, selection even in the absence of speciation is a rapid evolutionary process, so that the appearance and rapid selection of new variants might lead to the appearance of punctuated evolutionary change within a single species.

Indeed, given the speed of natural selection, slow evolutionary changes may be less common than rapid ones. Nevertheless, there are many examples of slow changes in the fossil record, a pattern called gradualism.

Adaptive radiation

Sometimes, large numbers of speciations in a single group of animals happen at once. The new populations generated by this burst of speciations often are variable in their adaptations to the environmental niches they occupy, as well as in their anatomical and behavioral makeup. Such a burst of speciation is called an adaptive radiation.

Adaptive radiations can happen whenever the reproductive success of a population brings it into contact with new environments in which its members are able to adapt and succeed. For example, the evolution of the four-chambered stomach in the ancestors of antelopes and cattle allowed them to use grasses that were not well used by other herbivores. This adaptation allowed their descendants to radiate into many different niches based on their ability to digest this material, leading to their extensive diversity today, which ranges from tiny Thompson's gazelles to large bison. No one species could occupy all these specialized niches. But in competition with each other, as well as with other species, populations of the original bovid quickly diverged to encompass these adaptations and others. This original adaptive radiation was therefore enabled by the evolution of the digestive system, which provided new energetic and dietary opportunities for bovid species.

Although the great apes today include only a small number of species, apes in the past were much more numerous. One of the reasons underlying this great collapse of ape diversity is the success of the Old World monkeys, which compete with apes for resources in forest environments. The Old World monkeys themselves underwent a substantial adaptive radiation during the Middle Miocene, capitalizing on their great dietary breadth, partly marked by their effective shearing molars, as well as their relatively short birth intervals compared to the apes. As climatic shifts became more rapid and frequent during the Late Miocene, the apes lost further ground to the monkeys, who underwent at least one more adaptive radiation based on the gut specializations toward leaf eating in the colobine monkeys. The evolution of important adaptations--especially those that enable exploitation of new food resources--is an important reason for the success of some lineages.

Sometimes, an adaptive radiation may result from an old adaptation that leads to new opportunities. For example, animals may colonize new areas, exposing many new niches in which they can out-compete other animals. The arrival of monkeys in South America is one such case, in which the combination of placental birth and arboreal adaptation caused these primates to succeed and diversify over many indigenous marsupials and birds. In other cases, an adaptive radiation may occur when an adaptation becomes useful in a broad range of environments. Bipedal locomotion in hominids is an example. Bipedalism may have evolved to allow efficient above-branch walking or walking short distances between groups of trees, but proved very effective in the more open woodlands of the early Pliocene, possibly leading to a radiation of different bipedal species.

Competitive exclusion

One of the patterns of macroevolution is competitive exclusion, which governs the outcome of competition between species for a limiting resource (Hardin 1960). Many natural populations coexist without dire consequences, because they depend on different resources, or are not limited in numbers by the resources that they share. But a limiting resource, the supply of which directly limits the number of individuals that can exist in a population, cannot be shared by two populations without competition. If two populations depend on the same rare food source, or if the activities of one species place the requirements of another in jeopardy, the populations can react in three possible ways:

1. One of the populations moves away.
2. One of the populations changes its adaptation to reduce its dependence on the resource.
3. One of the populations becomes extinct.

The principle of competitive exclusion, described by these three predictions, implies that at most one of the populations can remain unchanged.

Often competitive exclusion occurs when exotic animals move into a new area, competing with native groups. For example, the introduction of dingoes into Australia caused them to come into competition with native marsupial carnivores for prey species. The outcome is a product of the long evolutionary histories of both kinds of mammals, which left the dingo with certain advantages over the native carnivores, leading to their extinction. Such extinctions are a regular pattern of macroevolution.

See also:

Species concepts

Phylogenies

References:

Eldredge N, Gould SJ. 1972. Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf J, editor, Models in paleobiology. San Francisco: Freeman and Cooper. p 82-115.

Flynn JJ, Wyss AR. 1998. Recent advances in South American mammalian paleontology. Trends Ecol Evol 13:449-454.

Hardin G. 1960. The competitive exclusion principle. Science 131:1292-1297.

Warren KS, Verschoor EJ, Langenhuijzen S, Heriyanto, Swan RA, Vigilant L, Heeney JL. 2001. Speciation and intrasubspecific variation of Bornean orangutans, Pongo pygmaeus pygmaeus. Mol Biol Evol 18:472-480.

A new population that results from a speciation event is called a species. But although species result from a simple process, recognizing species in nature can be complicated. Biologists cannot travel in time to observe the speciations that resulted in today's diversity of life, so they must observe the reproduction of living organisms to determine the makeup of species. Paleontologists can find the fossil evidence of the ancestors of today's species, but they cannot observe whether those fossil organisms could reproduce with each other. Because scientists have different kinds of evidence about organisms, they use different concepts of species when testing hypotheses about their evolution.

Biological species

The most obvious property that helps to define species is reproductive isolation. Biologists studying living animals often use the biological species concept, which envisions a species as a "group of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups" (Mayr 1942). It is the biological species concept that primatologists use to grapple with whether chimpanzees and bonobos are different species, for example, by observing the differences in their reproductive behaviors and the strength of geographic isolation between their populations.

The biological species concept has some important limitations for paleontology. Making use of the concept depends on observing the mating behavior and interbreeding patterns of animals in their natural environments, which is not possible with fossils of organisms that lived in the past. Other kinds of observations that paleontologists might gather, such as morphological differences between fossils, have no necessary value under this concept. Another limitation is that the biological species concept does not incorporate any idea of how species may change over time. Paleontologists study fossils that may be separated by hundreds of thousands of years of time. It is difficult to imagine such widely separated individuals as part of the same reproductive community, even if they were very similar to each other. Over such time periods, evolution can transform populations substantially. The biological species concept recognizes the genetic continuity within a species caused by gene flow, but it does not incorporate a view of species existing over evolutionary time. For these reasons, paleontology requires a different kind of species concept.

Phylogenetic species concept

The phylogenetic species concept is an attempt to define species by their relationships to other species. Instead of trying to determine the reproductive boundaries of populations, scientists using the phylogenetic species concept attempt to uncover their genealogical relationships. A group of individuals that includes all the descendants of one common ancestor, leaving no descendants out, is called a monophyletic group.

Paleontologists Niles Eldredge and Joel Cracraft devised a species concept called the "Phylogenetic Species Concept," intended to apply to circumstances in which reproduction or isolation among organisms could not be observed. Under this concept, a species is "a diagnosable cluster of individuals within which there is a parental pattern of ancestry and escent, beyond which there is not, and which exhibits a pattern of phylogenetic ancestry and descent among units of like kind" (Eldredge and Cracraft 1980:92).

Key to the phylogenetic species concept is the idea that species must be "diagnosable." In other words, members of the species should share a combination of characteristics that other species lack. To look for the unique features that define a phylogenetic species, paleontologists must perform systematic comparisons with other related fossils or living species. These aspects of the concept make it widely applicable in paleontology.

But the phylogenetic species concept is not without its problems. Because the concept defines species based on morphology, without explicitly referring to populations or reproductive boundaries, it does not apply well to cases where morphologically different populations are connected by gene flow. Morphological variation among populations is not uncommon within living species. Humans today are a species with substantial morphological variation from continent to continent. Humans on different continents are not reproductively isolated, and their variation is largely distributed as clines over large geographic distances. Yet a paleontologist who had only a few fragmentary specimens from each continent would not necessarily know the pattern of variation, and many features of his specimens would appear to be unique. What would the paleontologist make of the high nose of a European specimen, the forward-facing cheeks of an Asian fossil, or the strong browridge above the eye orbits of an Australian, each taken randomly from their variable populations? By applying the phylogenetic species concept, a paleontologist would probably conclude that the different continents were homes to different human species.

Thus, because the phylogenetic species concept does not identify species based on the reproductive boundaries between them, it may have the effect of identifying populations connected by gene flow as different species. For this reason, a phylogenetic species as defined by a paleontologist may not correspond to a real prehistoric population that was the product of a speciation. Some paleontologists do not view this potential conflict as a problem, because identifying species based on unique characteristics will create as full as possible a systematization of the evolution of new features. Assuming that the number of ancient species was very large, and the number of fossils representing each of them is very small, then paleontologists can hardly hope to identify every speciation event in the past. The phylogenetic species concept may therefore provide a better approximation of the number and diversity of species that existed than other alternatives.

On the other hand, identifying populations connected by gene flow as different species can be a significant problem for paleontologists who take a greater interest in the processes of evolution than in the diversity of species in the past. Gene flow is a significant force shaping evolutionary change within populations. Moreover, evolution may cause a single species to change over time, possibly acquiring new unique features without any division of a species into separate reproductively isolated populations. Some paleontologists approach these difficulties by altering their view of the evolutionary process. If speciations can happen as a transformation of a single population in addition to the appearance of reproductive boundaries between populations, then a single evolving population may over time comprise several phylogenetic species. Or if most evolutionary change happened at the time of speciation, as asserted by the concept of punctuated equilibrium, then the phylogenetic species concept might more closely approximate the actual pattern of speciations in the past. But without such assumptions, the phylogenetic species concept's problems sometimes create a stumbling block for some paleontologists in attempting to understand the evolutionary process.

Evolutionary species

The evolutionary species concept combines the genealogical basis of the phylogenetic species concept with the genetic basis of the biological species concept. An evolutionary species is a lineage of interbreeding organisms, reproductively isolated from other lineages, that has a beginning, an end, and a distinct evolutionary trajectory (Wiley 1978). The beginning of a species' existence is a speciation, as a population becomes reproductively isolated from a parent population. The end of a species occurs either with extinction or with the branching of the species into one or more descendants.

Central to the evolutionary species concept is the idea of an evolutionary trajectory. The trajectory of a species is the evolutionary pattern of its characteristics over time. For example, one of the earliest species in the story of human evolution, Australopithecus afarensis, is represented by dozens of fossil teeth and mandibles, as well as other remains. Paleontologists hypothesize that these fossils, from several sites in East Africa, are members of a single species because of their many morphological resemblances. No very similar fossils have ever been found before 3.6 million or after 3 million years ago, dates that appear to indicate the beginning and the end of the species.

Nevertheless, the fossils do show some differences that appear over time. Although the molar teeth of the fossils do not change over time, the mandibles are thicker and more massive in more recent fossils than in the most ancient ones. As far as paleontologists can test, the mandibles form a single series evolving over time toward greater size and thickness. The evolutionary species concept infers that the fossils represent a species, beginning 3.6 million years ago and ending 3 million years ago, with an evolutionary trajectory that includes the evolution of greater mandibular thickness, without apparent changes in molar sizes.

The strength of the evolutionary species concept is that it allows paleontologists to focus on the causes of evolutionary change, whether they occur during speciations or at other times. Regarding A. afarensis, the observation that mandibles increased in size during the existence of the species may be explained by different evolutionary forces and conditions than if all the change occurred with the reproductive isolation of a new population. Although the greater mandibular thickness of later mandibles might be a unique feature, attempting to establish a new phylogenetic species for the later fossils might detract from an explanation of the overall evolutionary pattern.

Phylogenetic species vs. evolutionary species concepts

But the evolutionary species concept also has its problems. Because it uses several different criteria, much more information may be necessary to define an evolutionary species. Some scientists do not view this as a drawback, since even if a scientific view of the species that once existed and their boundaries and relationships proves a challenge, it may nevertheless add to our understanding of the evolutionary process.

Yet for many paleontologists, the need to amass great numbers of fossils from different times makes the evolutionary species concept nearly impossible to implement. At the same time, if scientists always hold out the possibility that two different fossils were actually connected by gene flow, it may impede an understanding of evolutionary changes that accompany the appearance of new reproductively isolated species. If we want to have a scientific, meaning falsificationist, view of the species that have existed and their boundaries and relationships to each other, we must accept that the process will in many cases be difficult. Simply making up many species hypotheses cannot add to our knowledgeÑand in many cases it may detract. What is important is that we realize that our record of past species is incomplete, and our failure to substantiate the existence of many species in the past does not constitute evidence that they did not exist.

Testing species hypotheses

However species are defined, whenever scientists identify a species, they actually are stating a hypothesis about the relationships among individual organisms. Such a hypothesis may be tested using morphological, genetic, or behavioral evidence. Discovering real species that existed in the past involves predicting the morphological variability of populations, including variation that occurs among populations connected by gene flow. In the relatively small fossil samples available to paleontologists, determining the number of species in a sample is a significant problem. Researchers use a number of techniques to test species hypotheses with limited morphological samples.

Two fossil hominids: different species or not?

1. What is the level of morphological difference between two or more specimens? Using a living species for comparison, scientists can determine the likelihood of sampling similar variability as the fossil sample (Miller 2000).
2. What are the relative frequencies of characteristics in two samples of fossils? Statistical comparison with the differences between different populations within a living species can determine whether the differences in frequencies observed in the fossils would be likely to occur within the comparison species. Such comparisons can be extended to the differences between the sexes of a living species to test whether sexual dimorphism accounts for differences between fossils (Lee 1999).
3. How do morphological features covary? If one fossil sample has a high incidence of several features that are absent or at low frequency in another sample, this supports the hypothesis that the two samples represent different species. With samples of sufficient size, say, 10 individuals or more, paleontologists can even estimate the maximum level of gene flow consistent with the morphological differences, and thereby frame a test of the hypothesis of different species in solid evolutionary terms (Hawks and Wolpoff 2001).
4. Do samples represent change over time? Sometimes paleontologists can use different populations from living species to evaluate likelihood that certain kinds of changes might occur over time. The best comparisons are with large samples of fossils that represent long spans of time, however. Although the evolutionary process is in ways unique for each species, analyses of the rate and level of changes in other species provide the most powerful tests of species hypotheses available in studying the past.

References:

Eldredge N, Cracraft J. 1980. Phylogenetic patterns and the evolutionary process: Method and theory in comparative biology. New York: Columbia University Press.

Hawks J, Wolpoff MH. 2001. The accretion model of Neandertal evolution. Evolution 55:1474-1485.
PubMed

Lee SH. 1999. Evolution of human sexual dimorphism: Using assigned resampling method to estimate sexual dimorphism when individual sex is unknown. Ph.D. thesis, University of Michigan.

Mayr E. 1942. Systematics and the origin of species from the viewpoint of a zoologist. New York: Columbia University Press.

Miller JMA. 2000. Craniofacial variation in Homo habilis: An analysis of the evidence for multiple species. Am J Phys Anthropol 112:103-128.
PubMed

Wiley EO. 1978. The evolutionary species concept reconsidered. Syst Zool 27:17-26.