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Gene flow and species delimitation

https://doi.org/10.1016/j.tree.2009.02.011Get rights and content

A defining feature of species is that their constituting populations are connected by gene flow. However, interspecific gene flow (introgression) can affect species integrity. If some genome components were less prone to introgression than others, they should be particularly suitable to delimitate species. Recent simulation studies have predicted a negative correlation between intra- and interspecific gene flow, suggesting that markers associated with the most dispersing sex should better delimitate species. A review of studies of introgression in species with sex-biased dispersal largely confirms this prediction. Hence, species delimitation should be more effective with markers experiencing high levels of gene flow, a simple but not widely appreciated prediction.

Introduction

Species delimitation, the methodological problem of identifying the boundaries between a set of species and therefore inferring the number of extant species, is an old issue that has recently attracted renewed attention 1, 2. Species are a cornerstone of biology, ecology and conservation, so their correct delimitation is essential, as illustrated by the surge of interest in barcoding approaches 3, 4, 5, 6. When selecting genetic markers for delimiting species, researchers have mostly focussed on their variability (e.g. [7]). A neglected criterion is the level of gene flow experienced by the markers. This is surprising because gene flow is a defining feature of species (see Box 1), and its role in species cohesion has been recently reiterated 8, 9. Moreover, due to the prevalence of sex-biased dispersal [10], different DNA regions are subject to varying levels of gene flow as a consequence of their mode of inheritance (biparental, maternal or paternal). It seems therefore logical to consider the effect of gene flow and not only mutation rate or effective population size when selecting markers for species identification and delimitation. In this paper, we suggest and attempt to test the idea that genome components experiencing high rates of gene flow should be better suited for species delimitation than those experiencing low rates of gene flow, in part because high rates of intraspecific gene flow can prevent introgression.

Section snippets

High gene flow markers to delimitate species?

The challenge in molecular taxonomy is to distinguish species that have low levels of genetic divergence, either because speciation is recent or because the species continue to exchange genes. Although it is legitimate to try to detect introgressed individuals using appropriate markers (see Ref. [11] for a comparison of existing methods to detect hybrids), identifying reproductive entities using genome components that introgress less readily than the rest of the genome (and hence might not be

Testing the prediction

To evaluate the relevance of this prediction, we compiled data on rates of introgression for at least two types of markers having different modes of inheritance (i.e. mitochondrial DNA [mtDNA], sex chromosomes or autosomes). We focussed on wild species for which sex-biased dispersal had been established or could be inferred. Three animal classes were considered, mammals (where many species have male-biased dispersal 10, 14), birds (where many species have female-biased dispersal 10, 15) and

Other interpretations of marker-specific rates of introgression

Haldane's rule [24], which states that ‘when in the offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterogametic sex,’ is the most frequent explanation for the heterogeneity of introgression rates at markers with contrasted modes of inheritance, because it implies that markers transmitted only by the heterogametic sex will be less introgressed. Our survey included 17 cases where the female is the heterogametic sex (ZW, birds and Lepidoptera) and 20

Perspectives for species delimitation

Our counterintuitive prediction that markers experiencing more intraspecific gene flow should have more difficulty in crossing species barriers seems to apply broadly. Alternative explanations for observed differences in introgression rates among markers have less explanatory power, even though they might be valid in specific cases. The model we propose does not rely on selective processes, and should therefore be considered as a null neutral model that could be useful for hypothesis testing.

Perspectives for studies of speciation

The ideas reported in this paper emerged while studying the demo-genetic processes taking place during species interactions in the context of range shifts and expansions. Our findings suggest that previously assumed relationships between intra- and interspecific gene flow were seriously misleading, because they did not take into account the spatial and dynamic aspects of species hybridisation. The process we have outlined here provides a mechanistic basis for the recent observation that

Acknowledgements

We thank Guy Hoelzer and Rich Drewes for providing Figure I of Box 1, Ferran López, Elena Patriarca and Paolo Debernardi for providing the photographs shown in Box 3, Matt Barker for discussions on the role of gene flow in species concepts, and four anonymous referees for suggestions that helped improve our paper. R.J.P. was supported by the European Commission Network of Excellence EVOLTREE and R-Syst, a network of molecular taxonomists at INRA. L.E. was supported by Swiss NSF grant

Glossary

Allopatric
refers to the geographic separation of different populations.
Assignment method
any of several related statistical methods using genetic information to ascertain population membership of individuals.
Barcoding
the use of short, standardised DNA sequences to quickly and easily identify and discover species.
Cellular automata
discrete models consisting of a regular grid of cells, each in one of a finite number of states; the state of a cell is a function of the states of neighbouring cells in

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