Recent advances in assessing gene flow between diverging populations and species
Introduction
If one discovers that two species are not reproductively isolated but have actually been hybridizing and exchanging genes, what is the first question to ask? For some practical concerns, the relevant question is the semantic one of ‘should they be identified as separate species?’. But a more basic evolutionary question is ‘how did the species separate from each other if they have been exchanging genes?’ Species are nearly always identified because some kind of divergence (e.g. morphological or genetic) from other species has been discovered. We also know that it only takes a small amount of gene flow to keep two populations from diverging [1]. So if divergence has happened and gene exchange has also been happening, then there is a conundrum.
The general answer to the puzzle is that divergence can happen at some genes, even if there is gene exchange for other genes. Hybrids carry a full set of genes from each population, but backcross hybrids do not, and so it is possible for some genes to pass between populations if backcross hybrids vary in their fitness depending on which genes they carry. In this way, natural selection, acting differently in two diverging populations, can prevent gene flow at some genes (i.e. the genes at which divergence is occurring) and can enable other genes to pass between the populations. In other words, divergence in the presence of gene exchange implies that natural selection is playing an active role in the divergence process [2, 3, 4].
This review covers recent developments and applications in the detection and estimation of gene flow between species that have recently diverged. Given that a number of studies have found evidence for gene flow, it appears that divergence and speciation may often occur in the presence of gene flow.
Section snippets
Population genetics and divergence
When one population separates into two, genetic variation will be shared for some period of time even in the absence of gene exchange [5, 6, 7]. Figure 1 shows an example of how genealogies are more likely to coalesce within species if separation times are longer ago. If the sizes of both populations are large, and gene trees are deep within populations, then genealogies and genetic variation might be shared at some genes for very long periods of time, possibly even after the populations have
Gene flow revealed by differences among genes
If population genetic data are available from multiple loci, for each of two divergent populations or species, then the patterns of variation at the different genes can be contrasted with one another. A history of divergence with gene flow is generally indicated if some loci show little divergence and others show a large amount of divergence, such that the variation in divergence among the different genes is greater than expected under a model without gene flow [8].
In recent years, findings of
Statistical approaches to inferring gene flow
Figure 2 shows a graphical model that represents an ancestral population that split, at a specific point in time, into two populations, after which there might have been gene exchange in one or both directions. The model can be represented in mathematical terms by six parameters, including the effective population sizes of the ancestral and descendant populations (NA, and N1 and N2, respectively), the splitting time (t), and two gene-flow parameters (m1 and m2). Called the ‘isolation with
An example from chimpanzees
Figure 3 shows examples of migration parameter curves for the central and western subspecies of common chimpanzee, Pan troglodytes troglodytes and Pan troglodytes verus, respectively [26]. In the case of gene flow from P. t. troglodytes to P. t. verus, the curve has a peak near zero, and the probability of the peak is very near to what the probability is at zero. In this case, we cannot reject a migration rate of zero. However, in the reverse direction, the peak is far from zero, and the
Separate migration rates for different genes
A variation on the basic six-parameter method is to fit a model in which every locus in the dataset is provided with a pair of gene-flow parameters [30]. This model can explicitly incorporate the differential gene flow that is expected if gene flow and divergence are both occurring. Bull et al. [31•] studied two of the three Heliconius species (Heliconius cydno and Heliconius melpomene) studied by Kronforst et al. [28], and also found evidence for gene flow. However, in this case, by running a
Conclusions: understanding speciation
These recent findings of gene flow between divergent populations and species seem to suggest that gene flow is a common feature of the early stages of the divergence process. This is surprising for two reasons. First, these examples come not from populations that have recently separated but from different populations or species that have been clearly identified on the basis of divergence. Second, it has at times been claimed that gene flow is rare or non-existent between populations that
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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