Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species

Genome-scale scans have revealed highly heterogeneous levels of divergence between closely related taxa in many systems. Generally, a small number of regions show high differentiation, with the rest of the genome showing no or only low levels of divergence. These patterns have been interpreted as evidence for ongoing speciation-with-gene-flow, with introgression homogenizing the whole genome except loci involved in reproductive isolation. However, as the number of selected loci increases, the probability of introgression at unselected loci decreases unless there is a transmission ratio distortion causing an over-representation of specific combinations of alleles. Here we examine the transmission of three 'speciation islands' that contain fixed differences between the M and S forms of the mosquito, Anopheles gambiae. We made reciprocal crosses between M and S parents and genotyped over 2000 F 2 individuals, developing a hierarchical likelihood model to identify specific genotypes that are under-or over-represented among the recombinant offspring. Though our overall results did not match the expected number of F 2 genotypes, we found no biased co-transmission among M or S alleles in the three islands. Our likelihood model did identify transmission ratio distortion at two of the three islands, but this distortion was small (approx. 3%) and in opposite directions for the two islands. We discuss how our results impinge on hypotheses of current gene flow between M and S and ongoing speciation-with-gene-flow in this system.

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

No evidence for biased co-transmission of speciation islands inAnopheles gambiae

Hahn

White

Muir

et al. 2012

“…Conversely, selection can also act simultaneously on many physically unlinked genomic regions. Under this view, genomes are highly porous and islands of speciation, as small as a single gene, are scattered throughout the genome [7,9,13,14]. Both scenarios may act concurrently, as large regions of differentiation are created while, simultaneously, selection isolates single genes or mutations from the homogenizing effects of gene flow.…”

Section: The Nature Of Genomic Islands Of Divergencementioning

confidence: 99%

“…Chromosomal rearrangements are one genetic mechanism that may promote the initial appearance and further spread of genomic islands of divergence [8,14,15]. These rearrangements are expected to impede gene flow through the suppression of recombination around chromosomal breakpoints, thus promoting the growth of diverging regions and ultimately facilitating speciation.…”

Section: The Nature Of Genomic Islands Of Divergencementioning

confidence: 99%

Genome-wide patterns of divergence during speciation: the lake whitefish case study

Renaut

Maillet

Normandeau

et al. 2012

103

117

The nature, size and distribution of the genomic regions underlying divergence and promoting reproductive isolation remain largely unknown. Here, we summarize ongoing efforts using young (12 000 yr BP) species pairs of lake whitefish (Coregonus clupeaformis) to expand our understanding of the initial genomic patterns of divergence observed during speciation. Our results confirmed the predictions that: (i) on average, phenotypic quantitative trait loci (pQTL) show higher F ST values and are more likely to be outliers (and therefore candidates for being targets of divergent selection) than nonpQTL markers; (ii) large islands of divergence rather than small independent regions under selection characterize the early stages of adaptive divergence of lake whitefish; and (iii) there is a general trend towards an increase in terms of numbers and size of genomic regions of divergence from the least (East L.) to the most differentiated species pair (Cliff L.). This is consistent with previous estimates of reproductive isolation between these species pairs being driven by the same selective forces responsible for environment specialization. Altogether, dwarf and normal whitefish species pairs represent a continuum of both morphological and genomic differentiation contributing to ecological speciation. Admittedly, much progress is still required to more finely map and circumscribe genomic islands of speciation. This will be achieved through the use of next generation sequencing data but also through a better quantification of phenotypic traits moulded by selection as organisms adapt to new environmental conditions.

“…Importantly, however, D xy is expected to behave differently under models of selection at linked sites compared with models of speciation (table 1 and figure 1) [51]. Gene flow will reduce D xy in regions of high recombination (figure 1a).…”

Section: Recombination Rate Variation and Models Of Differentiation (mentioning

confidence: 99%

Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice

Nachman

Payseur

2012

347

477

Recently diverged taxa may continue to exchange genes. A number of models of speciation with gene flow propose that the frequency of gene exchange will be lower in genomic regions of low recombination and that these regions will therefore be more differentiated. However, several population-genetic models that focus on selection at linked sites also predict greater differentiation in regions of low recombination simply as a result of faster sorting of ancestral alleles even in the absence of gene flow. Moreover, identifying the actual amount of gene flow from patterns of genetic variation is tricky, because both ancestral polymorphism and migration lead to shared variation between recently diverged taxa. New analytic methods have been developed to help distinguish ancestral polymorphism from migration. Along with a growing number of datasets of multi-locus DNA sequence variation, these methods have spawned a renewed interest in speciation models with gene flow. Here, we review both speciation and population-genetic models that make explicit predictions about how the rate of recombination influences patterns of genetic variation within and between species. We then compare those predictions with empirical data of DNA sequence variation in rabbits and mice. We find strong support for the prediction that genomic regions experiencing low levels of recombination are more differentiated. In most cases, reduced gene flow appears to contribute to the pattern, although disentangling the relative contribution of reduced gene flow and selection at linked sites remains a challenge. We suggest fruitful areas of research that might help distinguish between different models.