P0800261_01 7/14/05 8:00 AM Page 3 C HAPTER 1 The Taxonomy of Primates T HE T in the Laboratory Context AXONOMY OF P Colin Groves RIMATES School of Archaeology and Anthropology, Australian National University, Canberra, ACT 0200, Australia 3 What are species? D Taxonomy: EFINITION OF THE The biological Organizing nature species concept Taxonomy means classifying organisms. It is nowadays commonly used as a synonym for systematics, though Disagreement as to what precisely constitutes a species P strictly speaking systematics is a much broader sphere is to be expected, given that the concept serves so many RIMATE of interest – interrelationships, and biodiversity. At the functions (Vane-Wright, 1992). We may be interested basis of taxonomy lies that much-debated concept, the in classification as such, or in the evolutionary implica- species. tions of species; in the theory of species, or in simply M ODEL Because there is so much misunderstanding about how to recognize them; or in their reproductive, phys- what a species is, it is necessary to give some space to iological, or husbandry status. discussion of the concept. The importance of what we Most non-specialists probably have some vague mean by the word “species” goes way beyond taxonomy idea that species are defined by not interbreeding with as such: it affects such diverse fields as genetics, biogeog- each other; usually, that hybrids between different species raphy, population biology, ecology, ethology, and bio- are sterile, or that they are incapable of hybridizing at diversity; in an era in which threats to the natural all. Such an impression ultimately derives from the def- world and its biodiversity are accelerating, it affects inition by Mayr (1940), whereby species are “groups of conservation strategies (Rojas, 1992). In the present actually or potentially interbreeding natural popula- context, it is of crucial importance for understanding tions which are reproductively isolated from other such laboratory primates and their husbandry. groups” (the Biological Species Concept). Mayr never The Laboratory Primate Copyright 2005 Elsevier ISBN 0-1208-0261-9 All rights of production in any form reserved P0800261_01 7/14/05 8:00 AM Page 4 actually said that species can’t breed with each other, with which they share their range (Carr and Hughes, indeed he denied that that this was in any way a neces- 1993). Evidently in the not-too-distant past blacktail sary part of reproductive isolation; he merely said that, females joined whitetail breeding herds and, while the under natural conditions, they don’t. whitetail phenotype was strongly selected for, the black- Reproductive isolation, in some form, stands at the tail mtDNA has remained in the population, fossil basis of what a species is. Having said this, it must be documentation of the hybridization event. admitted that it is no longer possible to follow Mayr’s In Primates, also, there are examples of hybridiza- concept as definitive. In a recent book (Groves, 2001, tion in the wild. A good example of the first case, see especially Chapter 3) I sketched the main reasons Cercopithecus ascanius (Redtail monkey) and C.mitis why this is so: (Blue monkey) in Uganda, has been described in detail by Struhsaker et al. (1988). The two monkeys, which • It offers no guidance for the allocation of allopatric are widely sympatric, meaning that they live in the same populations. areas over a wide range, interbreed at quite noticeable • Many distinct species actually do breed with each levels, yet remain separate and clearly distinguishable other under natural conditions, but manage to and no one has ever proposed to regard them as any- remain distinct. RIMATES thing but distinct species. This case is not unlike that P • The interrelationships of organisms under natural of the North American deer, mentioned above. conditions are often (usually?) unknown. These are two examples – one non-Primate, one • Many species do not reproduce sexually anyway. Primate – of pairs of distinct species which manage to remain distinct over wide areas even though there is Allopatry gene-flow between them. Much more common (or, AXONOMY OF better, more readily documented) are cases where pairs T To say that two populations are allopatric means that of species occupy ranges that are largely separate but HE their geographic distributions do not overlap – they are T meet along their margins (parapatric), and interbreed entirely separate. This means that they do not have the where they do so. Interbreeding varies from occasional chance to breed with each other, even if they wanted to. 4 to full hybrid zones, and such cases have, unlike the There is, for example, no way of testing whether hybridization-in-sympatry cases, been regarded as evi- Macaca fuscata (of Japan), M.cyclopis (of Taiwan) and dence that reproductive isolation does not exist, so the M.mulatta (the Rhesus Macaque, of the East Asian two species should be merged into one. But there is mainland) are actually different species or not; they are ODEL no difference, in principle, from the hybridization-in- M classified as distinct species in all major checklists, but sympatry cases. there is no objective way of testing this classification The classic study of a hybrid zone is that of under the Biological Species Concept. two mice, Mus musculus and Mus domesticus, across RIMATE Indeed, this is the usual situation: populations that the Jutland peninsula, Denmark (see summary in P differ, in some respect, from one another and are, by Wilson et al., 1985). The hybrid zone, as measured relevant criteria, closely related are usually allopatric. by morphology and protein alleles, is very narrow; yet To take demonstrable reproductive isolation, the req- the mtDNA of the southern species, M.domesticus, uisite criterion under the Biological Species Concept, introgresses well across the boundary, and across the as the sine qua non of species status would be to leave seaway (the Skagerrak) into Sweden. This suggests the majority of living organisms unclassifiable except both that hybridization has been occurring, and that EFINITION OF THE by some arbitrary fiat. M.musculus has been expanding its range, and the D hybrid zone has been moving south since before the sea Natural interbreeding broke through separating Denmark and Sweden in the early Holocene. There has been no selection against The two common species of North American deer hybridization during this long period. (Odocoileus virginanus, the Whitetail, and O.hemionus, In a well-studied Primate example, two baboons, the Blacktail) are found together over a wide geo- Papio hamadryas (Hamadryas baboon) and P.anubis graphic area, and are always readily distinguishable; yet (Olive baboon), are parapatric and hybridize where molecular studies have found evidence that there has their ranges meet in Ethiopia, the hybrid zone being been hybridization. For example, in Pecos Country, not more than a few kilometres wide. The two taxa are west Texas, four out of the nine whitetails examined adapted to more arid and more mesic environments, had mitochondrial DNA characteristic of the blacktails respectively, and the hybrid zone travels up and down P0800261_01 7/14/05 8:00 AM Page 5 the Awash River according to whether there has been a an element of process, whereas the objective aspect is the run of dry seasons or a run of wet seasons, but remains mere existence of diagnosable difference. more or less the same width. This case is therefore not The second common misunderstanding is that unlike that of the two mice in Denmark. Unlike the species are now being defined by degree of difference. Cercopithecus example, the two baboon taxa have been They are not. They are being defined by the status of shuffled back and forth between subspecies and species the difference, whether the candidates for species status (compare Jolly, 1993 and Groves, 2001). Yet what is can be diagnosed or not. There is, for example, no stan- the difference, really? dard genetic distance above which species status is involved and below which it is not. The third misunderstanding is that species must still be in some way reproductively isolated. The interbreeding What are species? criterion obviously dies hard. The baboon example and others show that diagnosability exists irrespective of the T HE The phylogenetic persistence of the ability to hybridize. Their separateness T is genetic rather than necessarily reproductive. AXONOMY OF species concept Groves (2001) noted that some Primate taxono- mists have already begun employing the phylogenetic Most attempts to modify the definition of a species species concept, particularly those working on South have been modifications of the Mayr concept, and relied American monkeys, and made proposals as to what a on reproductive status (see Groves, 2001, Chapter 3). full classification of the order might look like. These P Even without the practical problems summarized proposals should be regarded as a first step and are not RIMATES above, such definitions seem inherently flawed because in any way intended as definitive. they appeal to the process of how species come to be, or are maintained, when surely they should be recognized by the pattern of what they actually are. It was put suc- What are subspecies? cinctly by Cracraft (1983): “Evolution produces taxo- 5 nomic entities, defined in terms of their evolutionary differentiation from other such forms. These entities Subspecies are geographic segments of species that dif- D should be called species . A species is the smallest fer from one another as a whole, but not absolutely. EFINITION OF THE diagnosable cluster of individual organisms within which The two criteria are: there is a parental pattern of ancestry and descent”. This • They are geographic populations (or groups of popu- is the Phylogenetic Species Concept. lations), not morphs within a single population.