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Is the Biological Species Concept Showing Its Age? Mohamed A.F

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Is the Biological Species Concept Showing Its Age? Mohamed A.F Research Update TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 153 Research News Is the biological species concept showing its age? Mohamed A.F. Noor A recent paper by Chung-I Wu in the Journal not been attained. Hence, such a strict and whether Wu’s proposed revision has of Evolutionary Biology questions the value definition would not match the intuition any advantages. Most of those who of the popular biological species concept of most biologists. Second, speciation responded on these issues were not (BSC) and offers an alternative ‘genic’ is usually driven by natural or sexual favorable to Wu’s proposal. concept based on possessing ‘loci of selection causing functional divergence. Wu presents examples in which the differential adaptation.’ Wu suggests that However, the BSC does not delineate the BSC delineates taxa as species that would recent empirical results from genetic studies evolutionary forces that cause divergence. not attain this designation under his genic of speciation necessitate this revision. As such, the BSC considers reproductively definition. For example, he notes that Several prominent evolutionary biologists isolated units to be species, even if taxa infected with different strains of responded in the same issue, many noting differential adaptation is not apparent. Wolbachia (hence preventing gene excitement over the recent empirical results, Wu proposes what he calls a ‘genic view exchange through cytoplasmic few agreeing with an abandonment of the of the process of speciation’. He suggests incompatibility) would be defined as BSC, and none wholeheartedly embracing that the point in divergence at which species by the BSC. Is this species the new genic concept. separate species should be recognized is assignment questionable, as Wu implies? ‘the stage where (1) the gene pools of loci A recent study reported two species of One reason why evolutionary biology of differential adaptation would not mix Nasonia that were isolated almost sometimes fails to gain the respect of other when the extrinsic barriers to gene exclusively by bidirectional Wolbachia scientists is because of its endless debates exchange are removed; and (2) the spread incompatibility [9], and clearly several over questions that focus on semantics. The of advantageous mutations are sometimes scientists in the evolution community did most famous (or infamous) of these involves (or often, but not always) restricted to not have a problem with this application of the definition of a species. Most biologists the population in which they originate. the BSC [10], because these Nasonia spp. think of species in terms of the biological Because the rest of the genome may mix are free to evolve independently [11]. species concept (BSC) [1,2], which defines upon contact, the genomes of the diverging Wu also argues that some taxa that species as interbreeding natural populations populations are expected to be mosaic in are considered to be true species by the that are reproductively isolated from other their extent of differentiation’. scientific community, such as Drosophila such populations. Thus, the acquisition of Several prominent biologists comment simulans and Drosophila mauritiana, have reproductive isolation is how adherents of on Wu’s proposal in the same issue, not attained species status according to the the BSC describe the process of speciation. including Ernst Mayr [5]. Several of these BSC. However, to make this argument, Wu However, many other concepts have been responses suggest that Wu’s points are not relies on a ‘strict isolation concept’, in which introduced and are championed by groups completely new. For example, in 1998, any gene flow negates the BSC. Many of biologists. Most of these concepts strive Feder [6] explicitly discussed many points cases exist of entities that are popularly to identify species in a manner that fits raised by Wu, including gene flow early in considered to be species but in which allele with our intuitive ideals: we desire the speciation process, the role of natural exchange occurs over some parts of the instinctively to have labeled categories that selection in speciation, and how an genome. Some of the responders to Wu’s explain the reality that we perceive [3]. extension of the BSC might be useful to paper felt that this was not a serious In a recent issue of the Journal of accommodate such observations. Feder impediment to accepting the BSC [12], Evolutionary Biology, Chung-I Wu revisits even refers to this revision as a reascension which considers speciation to be a process the species definition debate [4]. Wu has of Darwin’s view of speciation, as does Wu. rather than an event. Furthermore, any been at the forefront of genetic studies of Also, Mallet [7] suggested elsewhere that concept would surely fail when held to such reproductive isolation with an elegant species should be considered genotypic stringent interpretations. If we take Wu’s body of work on species and races in the clusters that can overlap spatially without concept to the extreme, populations of Drosophila melanogaster group. In the fusion, a revision of the BSC to allow for Drosophila pseudoobscura could be first paper of this issue, Wu stresses two some gene flow. considered to be separate species. Some conclusions that have emerged from None of the responders disagrees D. pseudoobscura populations exhibit recent studies and concludes that a with Wu’s first point, although animal fixed or nearly fixed differences in gene revision of the BSC is necessary to population geneticists (outside of those arrangement, and these differences appear accommodate them. First, several taxa studying hybrid zones) were slow to to be adaptive [13]. Following a ‘strict genic that biologists consider to be good species acknowledge it [8]. Similarly, no one species concept’, adaptive mutations in one exchange genes in some parts of their disagrees with Wu’s second point, and of these populations (if in the inverted genomes. A strict version of the BSC numerous other examples of speciation region) would not spread to other might assume that any gene exchange apparently driven by natural or sexual populations, and the gene pools within demonstrates that reproductive isolation selection are cited. The real issues are these arrangements do not mix. However, is incomplete and that species status has whether there is a need to revise the BSC extensive gene flow has been observed at http://tree.trends.com 0169-5347/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(02)02452-7 154 Research Update TRENDS in Ecology & Evolution Vol.17 No.4 April 2002 other parts of the genome among these on its extreme commonality [18]. Why 4 Wu, C-I. (2001) The genic view of the process of populations, suggesting that they do come should Wu’s concept be allowed such speciation. J. Evol. Biol. 14, 851–865 5 Mayr, E. (2001) Wu’s genetic view of speciation. into contact [14]. Unlike Wu’s example of glaring exceptions, whilst the BSC must J. Evol. Biol. 14, 866–867 taxa infected with differing strains of be employed in the strictest sense? There 6 Feder, J.L. (1998) The apple maggot fly, Wolbachia, the scientific community seems to be a double standard here, and Rhagoletis pomonella: flies in the face of considers these populations to be when Wu’s arguments encounter these conventional wisdom about speciation? In Endless conspecific. Many other examples could be special cases, he falls back on reproductive Forms: Species and Speciation (Howard, D.J. and Berlocher, S.H., eds), pp. 130–144, Oxford brought to bear where the BSC does not isolation [19]. Hence, Wu’s concept University Press assume speciation is complete but ‘loci of provides only a very limited, if any, 7 Mallet, J. (1995) A species definition for the differential adaptation’exist. conceptual advance. Modern Synthesis. Trends Ecol. Evol. 10, 294–299 Cases also exist in which the BSC would Finally, we are left with the question of 8 Rieseberg, L.H. and Burke, J.M. (2001) A genic properly define taxa as species but in which where such a debate leads us. On the one view of species integration. J. Evol. Biol. 14, 883–886 Wu’s genic concept would not. One example hand, species concepts determine how the 9 Bordenstein, S.R. et al. (2001) Wolbachia-induced of nonadaptive speciation is polyploidy. process of speciation is studied. Because incompatibility precedes other hybrid Polyploidy causes speciation within a few it is arguably the fundamental step in incompatibilities in Nasonia. Nature 409, 707–710 generations, but there are no ‘loci of cladogenesis and the generation of 10 van Alphen, J.J.M. (2001) Sexual selection, differential adaptation’[15]. Hence, Wu’s biodiversity, speciation has an reproductive isolation and the genic view of speciation. J. Evol. Biol. 14, 874–875 definition would consider diploids and indisputable role in evolutionary studies. 11 Bridle, J. and Ritchie, M.G. (2001) Assortative resultant auto- or allotetraploids to be On the other hand, only very limited mating and the genic view of speciation. J. Evol. conspecific, whereas the BSC considers scientific advances have emerged from Biol. 14, 878–879 them to be heterospecific. Similar problems the introduction of more species concepts, 12 Rundle, H.D. et al. (2001) Hybridization without guilt: gene flow and the biological species concept. hold in cases where chromosomal particularly when compared with the J. Evol. Biol. 14, 868–869 rearrangements contribute to speciation exciting empirical results of the past 13 Lewontin, R.C. et al. (1981) Dobzhansky’s Genetics [16]. In both of these scenarios, most 15 years. Lineage-based species concepts of Natural Populations I–XLIII, Columbia evolutionary biologists adopt the BSC even could provide some advantage for University Press though there is no indication of differential conceptualizing and classifying species, 14 Schaeffer, S.W.
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