Evolutionary Anthropology 23:5–7 (2014)

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Recognizing Species, Present and Past IAN TATTERSALL

Nobody disputes that nature is meaningfully “packaged” in some way. But debate persists over exactly how (and even whether) the boundaries dividing taxa should (can) be drawn. At one end of the scale, some zealots abstrusely deny real existence to higher taxa.1 At the other, laborers at the taxonomic rock-face confront genuine challenges in recognizing and delineating the species that systematists agree constitute the most fundamental unit of taxonomic analysis.2, 3

These difficulties exist at both conceptual and operational levels. In theory, they are independent, but they are liberally confused because operational considerations have often been allowed to feed back into species definitions. In other words, defining what species are in principle has too often been a matter of taxonomists’ convenience. This is one major reason why Coyne and Orr4 were recently able to list well over 30 definitions of the species in active current use. Nobody benefits from the consequent muddle, which is best sidestepped by adopting Ghiselins5 elegant characterization (not definition) of species as individuals. Surely we can all agree that species are, most fundamentally, the smallest historically and genomically individuated lineages of organisms. Yet the individuation of populations is often hard to confirm or deny. In large part, this is because

Ian Tattersall is a curator emeritus at the American Museum of Natural History. He has worked on lemur systematics and ecology as well as in paleoanthropology, where his special interest is in hominid diversity and cognitive evolution. [email protected]

Key words: speciation; species recognition; fossils; diversity; systematics

C 2014 Wiley Periodicals, Inc. V

DOI: 10.1002/evan.21385 Published online in Wiley Online Library (wileyonlinelibrary.com).

species are the products of speciation, and speciation is far from being a unitary process. Rather, it is something we recognize in retrospect: the effective cessation of genetic continuity among sister populations – their individuation – may be mediated by numerous different mechanisms that act at all levels, from the genomic to the anatomical and behavioral. As a result, there are many ways in which individuation may or may not express itself. This diversity of causation can make life difficult for systematists of all kinds, whether their subjects are living or extinct. For paleontologists, there is the supreme operational difficulty that speciation is not simply a passive consequence of morphological change.6 This discordance is particularly problematic because neither geological age nor geographical origin is a reliable key to the affinity of any individual fossil.7 At best, systematists can add these attributes to a probability assessment perforce based on morphology. Also, because of the disconnect between morphology and speciation in living primates, which furnish our only verifiable yardstick for judging the past, provide us with examples of both geographically widespread species with well-differentiated local populations and sympatric individuated species that don’t appear very different to the human eye.

Individuals, of course, possess their anatomical attributes by virtue of belonging to a particular species, so that a fossil’s hard-tissue anatomy should, in theory, be a robust indicator of its identity. But while this is true in principle, anatomical variation itself also varies widely among species,6 confounding simple statistical assessment of differentiation. Combined with the loose linkage between morphology and speciation, this inconvenient fact might seem to deprive morphology of yet more of its systematic sheen. Complicating things still further is the observation that, among most primates, morphological variation among species of the same genus tends to be expressed in external soft-tissue characteristics that do not impress themselves significantly on the durable bony tissues beneath. This leads to the odd result that, while it is undoubtedly species that split to generate new lineages, the most robust hard-tissue gestalt category is the genus. There is, then, no morphological silver bullet out there for recognizing species. Nonetheless, such awkward complicating factors as sexual dimorphism aside, it remains true that the consistent presence of a distinctive morphology in a subset of a fossil assemblage argues strongly in favor of independent species status for that subset. The implications for the primate paleontologist are clear. If closely related species tend to differ rather little in bony and dental morphology, there will be a tendency to underestimate the actual variety of species represented in fossil samples. From the systematist’s perspective, this bias is actually preferable to the alternative.

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For while a low estimate of species diversity will undeniably oversimplify the historical picture, unlike an overestimate, it will not actively distort perceived evolutionary patterns within the larger clade involved. In the hothouse of paleoprimatology, other significant factors are also at work. The boom-and-bust pattern, whereby species and genera accumulate within a clade and are then dramatically reduced before beginning to proliferate once more (Miocene apes are the classic example), exemplifies a Kuhnian phenomenon that is not only independent of the actual fossil evidence, but sometimes also independent of any species concepts that might have crept into the picture. The same may be said of the powerful historical biases that have, from the very start, promoted hyperlumping in paleoanthropology.8 For systematists trying to understand the structure of the living primate fauna, the operational – and philosophical – difficulties are very different from those in paleontology, although they are no less intractable for that. Speciation is a complex matter that may take considerable time to unfold completely. This makes it hard to discern sharp genetic boundaries between closely related populations that might occasionally interbreed if given the chance, but that are nonetheless already effectively individuated. On its own, then, cross-mating may have zero relevance for species status, while Mallet9 has even proposed that introgression between differentiated populations early in their existences can be an important influence on their subsequent evolution. For most students of the primates that live today in the world’s tropical forests and woodlands, internal hard-tissue morphology of the kind paleontologists depend on is at best a secondary systematic consideration. It is certainly not by virtue of the post-choanal pits in its cranial base, which are almost the only striking cranial autapomorphy to be found among all the species of Eulemur, that we recognize E. rubriventer as an individuated species. Just as important as that they look different to us is that, out there in the rainfor-

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est, red-bellied lemurs behave as a genetically independent entity. However, things are not always that simple. In the latest edition of the lemur Field Guide10 all of the former subspecies of Eulemur fulvus are recognized as species in their own right, for no better reason than that they differ among themselves in external characters that are readily visible to the observer. Yet they also have largely allopatric distributions and freely interbreed when given the opportunity. There is scant evidence that any of them has yet departed on its own individuated evolutionary

. . .while a low estimate of species diversity will undeniably oversimplify the historical picture, unlike an overestimate it will not actively distort perceived evolutionary patterns within the larger clade involved.

trajectory, as E. rubriventer so clearly has done. The rationale for splitting the fulvus-group in this way is furnished by the Phylogenetic Species Concept (PSC), which sees species as “irreducible cluster[s]. . . that [are] diagnosably distinct.”11 The PSC has also been used to justify the recognition of numerous more cryptic nocturnal lemur species (for example, of Microcebus and Lepilemur10) almost uniquely on the basis of mtDNA distances. Yet, while it is magnificently easy to apply, the PSC ignores the vital fact that the engine of new biodiversity is the emergence of distinct varieties within species. Without subspecies, there is no place for new species to start; and individuation will emerge independently, under other controls. Because of the dubious inflation of lemur species numbers engendered

by the PSC, the use of which typically increases species numbers by 50% compared to other species concepts,12 I have energetically advocated2,3 the use of a much broader range of criteria than simple diagnosability in recognizing living primate species. When inferring individuation, systematists should consider all available information, much as juries do in civil court (although, given the complexities of nature, the “beyond all reasonable doubt” criterion used in criminal court is probably asking too much). Such lines of evidence include morphology in its broadest sense, embracing superficial characters and olfactory signaling systems as well as internal anatomy; social behaviors; vocal and visual communication; DNA markers; geographical and ecological distributions; environmental preferences; and interactions with sympatric populations, including putative gene flow. Having tried over many decades to apply my experience of lemur systematics to understanding species diversity in the hominid fossil record, I find myself in a curious position. Among many students of the lemurs, I am known as a reactionary who is reluctant to acknowledge all the species diversity out there in the forests of Madagascar. Yet in paleoanthropology I am simultaneously seen as a crazy splitter who sees a new species under every rock. And then, of course, there is what I like to think of as the real me, trying to eschew both ideology and received wisdom and simply to be as judicious as I can in the face of the manifold difficulties that any alpha-taxonomist has to grapple with. Paleontology and neozoology both pose particular systematic challenges, some of which look insuperable in the near future. But one thing is clear: the effort to recognize species realistically has to be made. Basic systematics is far from being a humble clerical business that we should brush under the rug as fast as possible so we can get to the good stuff. Instead, it is what we must imperatively get right before we can say anything reliable at all, either

Recognizing Species, Present and Past 7

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about our ancestry or our current place in nature.

ACKNOWLEDGMENT My appreciation goes to John Fleagle for inviting me to contribute to this special issue of Evolutionary Anthropology.

REFERENCES 1 Cartmill M. 2013. The end of higher taxa: a reply to Tattersall. Evol Anthropol 22: 172–173. 2 Tattersall I. 2007. Madagascar’s lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol 16:12–23 (doi:10.1002/evan.20126).

3 Tattersall I. 2013. Understanding species-level primate diversity in Madagascar. Madagascar Conserv Dev 8:7–11. 4 Coyne JA, Orr HA. 2004. Speciation. Sunderland, MA: Sinauer Associates. 5 Ghiselin MT. 1974. A radical solution to the species problem. Syst Biol 23:536–544 (doi: 10.1093/sysbio/23.4.536). 6 Tattersall I. 1986. Species recognition in human paleontology. J Hum Evol 15: 165–175. (doi: 10.1016/S0047-2484(86)80043-4). 7 Eldredge N, Tattersall I. 1975. Evolutionary models, phylogenetic reconstruction, and another look at hominid phylogeny. In: Szalay FS, editor. Approaches to primate paleobiology. Basel: S. Karger. p 218–243. 8 Tattersall I. 2009. The fossil trail: how we know what we think we know about human evolution, 2nd ed. New York: Oxford University Press.

9 Mallet J. 2005. Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229–237. 10 Mittermeier RA, Louis EE Jr, Richardson M, et al. 2010. Lemurs of Madagascar. Arlington, VA: Conservation International. 11 Cracraft JL. 1983. Speciation concepts and speciation analysis. In: Johnson RF, editor. Current ornithology, vol. 1. New York: Plenum Press. p 159–187. 12 Agapow P-M, Bininda-Edmonds ORP, Crandall KA, et al. 2004. The impact of species concepts on biodiversity studies. Q Rev Biol 79: 161–179 (doi:10.1086/383542).

Multimodal Approach. New York: Cambridge University Press. 294 pp. ISBN: 9780521178358. $56.00 (paperback).  Nativ A. (2013). Prioritizing Death and Society:The Archaeology of Chalcolithic and Contemporary Cemeteries in the Southern Levant. Durham: Acumen Publishing. 301 pp. ISBN: 9781844657513. $120.00 (hardback).  Nelson C, Fox N, and Zeanah C. (2014). Romania’s Abandoned Children: Deprivation, Brain Development, and the Struggle for Recovery. Cambridge: Harvard University Press. 416 pp. ISBN: 9780674724709. $29.95 (hardback).

 Scheiber I, Weib B, Hemetsberger J, and Kotrschal K, editors (2013). The Social Life of Greylag Geese: Patterns, Mechanisms and Evolutionary Function in an Avian Model System. New York: Cambridge University Press. 237 pp. ISBN: 9780521822701. $99.00 (hardback).  Suddendorf T. (2013). The Gap: The Science of What Separates Us From Other Animals. New York: Basic Books. 358 pp. ISBN: 9780465030149. $29.99 (hardback).  Tomasello M. (2014). A Natural History of Human Thinking. Cambridge: Harvard University Press. 178 pp. ISBN: 9780674724778. $35.00 (hardback).

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Books Received  Finlay G. (2013). Human Evolution: Genes, Genealogies and Phylogenies. New York: Cambridge University Press. 359 pp. ISBN: 9781107040120. $75.00 (hardback).  Gurche J. (2013). Shaping Humanity: How Science, Art and Imagination Help Us Understand Our Origins. New Haven: Yale University Press. 368 pp. ISBN: 9780300185331. $49.95 (hardback).  Kennedy D. (2014). Plants and the Human Brain. New York: Oxford University Press. 379 pp. ISBN: 9780199914012. $59.95 (hardback).  Liebal K, Waller B, Burrows A, and Slocombe K. (2014). Primate Communication: A

Recognizing species, present and past.

Nobody disputes that nature is meaningfully "packaged" in some way. But debate persists over exactly how (and even whether) the boundaries dividing ta...
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