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Glittering gold and the quest for Isla de Muerta

2017; Oxford University Press; Volume: 30; Issue: 8 Linguagem: Inglês

10.1111/jeb.13110

1420-9101

Chris D. Jiggins, Simon H. Martin,

Genetic Mapping and Diversity in Plants and Animals

Journal of Evolutionary BiologyVolume 30, Issue 8 p. 1509-1511 CommentaryFree Access Glittering gold and the quest for Isla de Muerta C. D. Jiggins, Corresponding Author C. D. Jiggins c.jiggins@zoo.cam.ac.uk orcid.org/0000-0002-7809-062X Department of Zoology, University of Cambridge, Cambridge, UK Correspondence: Chris D. Jiggins, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK. Tel.: +44 1 223 269 021; fax: +44 1 223 336 676; e-mail: c.jiggins@zoo.cam.ac.ukSearch for more papers by this authorS. H. Martin, S. H. Martin Department of Zoology, University of Cambridge, Cambridge, UKSearch for more papers by this author C. D. Jiggins, Corresponding Author C. D. Jiggins c.jiggins@zoo.cam.ac.uk orcid.org/0000-0002-7809-062X Department of Zoology, University of Cambridge, Cambridge, UK Correspondence: Chris D. Jiggins, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK. Tel.: +44 1 223 269 021; fax: +44 1 223 336 676; e-mail: c.jiggins@zoo.cam.ac.ukSearch for more papers by this authorS. H. Martin, S. H. Martin Department of Zoology, University of Cambridge, Cambridge, UKSearch for more papers by this author First published: 08 August 2017 https://doi.org/10.1111/jeb.13110Citations: 10AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat The interpretation of patterns of divergence between related species across the genome is complex, and many of these complications are clearly reviewed in the article by Ravinet et al. (2017). Indeed, such a review is timely and clarifies much of the confusion about what can, and cannot, be inferred from such genome scans. Although the authors state that ‘We argue one of the principal aims of the field is to identify the barrier loci involved in limiting gene flow’, they also show how genome data can be used to investigate the genetic architecture of speciation without identifying individual barrier loci. We will argue that in many cases, the identification of barrier loci based on genomic data alone will be extremely challenging or impossible, and that it can be equally valuable to characterize general features of species barriers, such as their architecture and evolution through time. We caution against an obsession with the identification of functional loci that might distract researchers from addressing the many other exciting questions in speciation that do not require such specific information. Perhaps the first and most obvious reason why identification of barrier loci might be impossible is if the barriers themselves between species are highly polygenic. For example, it has long been known that a highly polygenic architecture, with many incompatibility loci of infinitesimal effect, can lead to a strong barrier to gene flow and ‘genome-wide congealing’ between hybridizing species (Barton & Bengtsson, 1986). In a hypothetical species pair isolated in this way, there would undoubtedly be considerable heterogeneity in FST across the genome. This could be due to random clustering of minor effect incompatibility loci, or due to variation in recombination rate, gene density, demographic stochasticity and all the other reasons outlined in the review article, but the search for particular barrier loci would be fruitless. As acknowledged by Ravinet et al., a similar argument can be made for loci involved in adaptation more generally: in speciation as in adaptation, it is likely to be the case that ‘All that is gold does not glitter’ (Rockman, 2012). Nonetheless, in many (perhaps most) species pairs, there are likely to be at least some barrier loci of major effect. In Heliconius butterflies, there is good evidence for major ‘speciation genes’. Wing pattern differences between species are controlled by a few large-effect loci and lead to strong pre- and post-mating isolation (Naisbit et al., 2003; Jiggins, 2008). Selection against hybrid butterflies is so strong that we can measure it in the field with simple experiments involving model butterflies (Merrill et al., 2012). These wing pattern loci were identified using traditional genetic approaches, and their genetic basis is now well understood. Nonetheless, when the genomes of strongly reproductively isolated species, such as Heliconius melpomene and Heliconius cydno, are compared, wing patterning loci do not stand out against the genomic background, despite ample evidence for gene flow between the species (Martin et al., 2013; Seehausen et al., 2014). FST across the genome is highly heterogeneous, with many ‘peaks’, which include but are not limited to wing pattern loci. Similar patterns are seen using dXY or other measures such as Fd which is a more unbiased measure of migration (Martin et al., 2015). As suggested by Ravinet et al., in the future, we can do better by accounting for genome-wide variation in patterns of recombination and selection, but we anticipate that some major effect barrier genes will remain indistinguishable in genome scans. In many cases, therefore, we will need some additional evidence to find barrier loci. These barriers may be like the Isla de Muerta in the Pirates of the Caribbean, which Jack Sparrow claimed ‘cannot be found except by those who already know where it is’. In contrast, between more closely related taxa, there are examples in which genome scans have identified highly divergent regions that contain functional ‘barrier genes’. These include hooded vs. carrion crows, freshwater vs. marine sticklebacks and divergent subspecies of Heliconius (Jones et al., 2012; Nadeau et al., 2012; Poelstra et al., 2014). A genome scan across many subspecies of the Heliconius erato radiation identified multiple narrow divergent regions that differentiate wing pattern races, representing modular regulatory loci around known wing patterning genes (Belleghem et al., 2017). All of these comparisons are between geographic forms in which background FST is close to zero, such that hybridizing populations are virtually panmictic across much of the genome. Another case in which a low background FST is combined with a relatively small number of divergent peaks are the sympatric cichlid fish in Lake Massoko (Malinsky et al., 2015) – an unusual case of sympatric species showing such a pattern. The search for barrier genes is therefore easier when taxa are very closely related and rates of hybridization are high. A further problem is the technical challenge of identifying narrow outliers against a noisy genomic signal. For example, Cruickshank and Hahn examined our data from Peruvian Heliconius wing pattern races, and did not find any peaks of divergence (dXY), suggesting little evidence for deeply divergent wing patterning alleles (Cruickshank & Hahn, 2014). However, subsequent fine-mapping has shown that causative alleles at the optix locus are in fact highly divergent. The ‘dennis’ locus diverged at the base of the whole clade of melpomene/silvaniform butterflies, some 4 million years ago perhaps an order of magnitude greater than the genomic divergence of H. m. amaryllis and H. m. aglaope. However, the causal locus for the ‘dennis’ patch is about 6 kb in extent, with a genotype–phenotype signal that rapidly decays in the surrounding genome (Wallbank et al., 2016). Such highly localized barriers are extremely hard to identify in genome scans, without additional evidence from mapping or expression studies. There is also an entirely opposite problem. Loci that contribute to species barriers may not have localized effects in the genome. Recent theory has shown that epistatic incompatibilities acting primarily against F1 hybrids can create weak but widespread barriers in the genome (Lindtke & Buerkle, 2015). Intuitively, any barrier that acts against early generation hybrids, before much recombination has occurred, will tend to have widespread effects, and may therefore never reveal its location. We suspect that the two major wing patterning loci that differentiate H. melpomene and H. cydno may act in this way, unlike in the within-species comparisons, where selection acts over a geographic cline. In general, theoretical work on this subject is dominated by models that assume that selection influences loci independently, with distinct environments being the major selective driver (Feder et al., 2012; Yeaman et al., 2016). However, most barriers, particularly between sympatric species, will be maintained by epistatic interactions among loci, with fitness determined by mis-matching alleles, rather than by a mismatch between allele and environment. Further theoretical work is needed to explore the consequences of epistasis for genome divergence. The goal of writing this response, however, is not to be relentlessly negative. Instead, we strongly encourage researchers embarking on a genome-scale study of speciation to identify other tractable questions. For example, to what extent is species divergence accompanied by ongoing gene flow? Ongoing gene flow provides unequivocal evidence for divergence and/or persistence with gene flow for at least part of the speciation process, addressing the age-old problem of sympatry vs. allopatry. This question is now readily tractable with an appropriate sampling design and a variety of statistics are available to estimate admixture, as summarized by Ravinet et al. (Box 3). In Heliconius, we have been astonished by the extent to which the genomes of sympatric species are influenced by admixture. This approach will be even more informative where similar comparisons can be carried out across a wide range of species pairs, increasing the generality of findings from a few focal taxa (Roux et al., 2016). Understanding the architecture, rather than the specific identity, of barriers to gene flow can in itself address long-standing questions in speciation biology. Theory predicts that patterns of admixture might be disproportionately located at the ends of chromosomes, on autosomes as compared to the sex chromosomes or in regions of high recombination (Barton & Bengtsson, 1986; Qvarnstrom & Bailey, 2008). The generality of these predictions can be tested now using genome-scale data, without the need for identification of specific barrier loci. For example, analysis of Neanderthal and human introgression has provided evidence for the role of background selection purging deleterious alleles as a pervasive force in shaping the patterns of admixture across the genome (Juric et al., 2016). A similar shift in emphasis has occurred in recent work on quantitative traits: some traits are so polygenic that we cannot hope to characterize most of the loci involved, but instead we can address relevant questions about the underlying genetic architecture of the trait without identifying specific loci (Yang et al., 2010). In summary, we caution against the proposal that the principal aim of the field is to identify barrier loci. Researchers embarking on a genome-scale study of closely related species should be prepared for the eventuality that it will be impossible to identify specific loci causing species-level divergence. 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