Special Issue "Evolutionary Genetics of Reproductive Isolation"

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (31 January 2018)

Special Issue Editors

Guest Editor
Professor Roger K. Butlin

Department of Animal and Plant Sciences, University of Sheffield, Room B83, Alfred Denny Building, Sheffield, UK
Website | E-Mail
Guest Editor
Dr. Isobel Eyres

Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK
E-Mail
Guest Editor
Dr. Anja Westram

Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK
E-Mail

Special Issue Information

Speciation requires the build-up of reproductive isolation. Strong isolation typically requires barriers to gene flow that influence a large proportion of the genome. Although recent work has provided exciting examples of the genetic basis of local adaptation or of genetic incompatibilities, the way in which multiple barriers accumulate to generate strong overall isolation remains largely a mystery. It may involve divergent selection across multiple dimensions, accumulation of incompatibilities, reinforcement, recombination suppression or other processes. This Special Issue aims to highlight the range of approaches currently in use to address the genetic basis of reproductive isolation, with a particular focus on the processes involved in evolving from an initial partial barrier to gene flow towards a genome-wide barrier.

Prof. Dr. Roger K. Butlin
Dr. Isobel Eyres
Dr. Anja Westram
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All papers will be peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Genes is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 1600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Published Papers (11 papers)

View options order results:
result details:
Displaying articles 1-11
Export citation of selected articles as:

Research

Jump to: Review, Other

Open AccessArticle The Genetic Architecture Underlying the Evolution of a Rare Piscivorous Life History Form in Brown Trout after Secondary Contact and Strong Introgression
Received: 1 February 2018 / Revised: 16 May 2018 / Accepted: 17 May 2018 / Published: 31 May 2018
PDF Full-text (2932 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
Identifying the genetic basis underlying phenotypic divergence and reproductive isolation is a longstanding problem in evolutionary biology. Genetic signals of adaptation and reproductive isolation are often confounded by a wide range of factors, such as variation in demographic history or genomic features. Brown
[...] Read more.
Identifying the genetic basis underlying phenotypic divergence and reproductive isolation is a longstanding problem in evolutionary biology. Genetic signals of adaptation and reproductive isolation are often confounded by a wide range of factors, such as variation in demographic history or genomic features. Brown trout (Salmo trutta) in the Loch Maree catchment, Scotland, exhibit reproductively isolated divergent life history morphs, including a rare piscivorous (ferox) life history form displaying larger body size, greater longevity and delayed maturation compared to sympatric benthivorous brown trout. Using a dataset of 16,066 SNPs, we analyzed the evolutionary history and genetic architecture underlying this divergence. We found that ferox trout and benthivorous brown trout most likely evolved after recent secondary contact of two distinct glacial lineages, and identified 33 genomic outlier windows across the genome, of which several have most likely formed through selection. We further identified twelve candidate genes and biological pathways related to growth, development and immune response potentially underpinning the observed phenotypic differences. The identification of clear genomic signals divergent between life history phenotypes and potentially linked to reproductive isolation, through size assortative mating, as well as the identification of the underlying demographic history, highlights the power of genomic studies of young species pairs for understanding the factors shaping genetic differentiation. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Open AccessArticle Transitions from Single- to Multi-Locus Processes during Speciation with Gene Flow
Received: 21 February 2018 / Revised: 16 May 2018 / Accepted: 17 May 2018 / Published: 24 May 2018
PDF Full-text (1797 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
During speciation-with-gene-flow, a transition from single-locus to multi-locus processes can occur, as strong coupling of multiple loci creates a barrier to gene flow. Testing predictions about such transitions with empirical data requires building upon past theoretical work and the continued development of quantitative
[...] Read more.
During speciation-with-gene-flow, a transition from single-locus to multi-locus processes can occur, as strong coupling of multiple loci creates a barrier to gene flow. Testing predictions about such transitions with empirical data requires building upon past theoretical work and the continued development of quantitative approaches. We simulated genomes under several evolutionary scenarios of gene flow and divergent selection, extending previous work with the additions of neutral sites and coupling statistics. We used these simulations to investigate, in a preliminary way, if and how selected and neutral sites differ in the conditions they require for transitions during speciation. For the parameter combinations we explored, as the per-locus strength of selection grew and/or migration decreased, it became easier for selected sites to show divergence—and thus to rise in linkage disequilibrium (LD) with each other as a statistical consequence—farther in advance of the conditions under which neutral sites could diverge. Indeed, even very low rates of effective gene flow were sufficient to prevent differentiation at neutral sites. However, once strong enough, coupling among selected sites eventually reduced gene flow at neutral sites as well. To explore whether similar transitions might be detectable in empirical data, we used published genome resequencing data from three taxa of Heliconius butterflies. We found that fixation index ( F S T ) outliers and allele-frequency outliers exhibited stronger patterns of within-deme LD than the genomic background, as expected. The statistical characteristics of within-deme LD—likely indicative of the strength of coupling of barrier loci—varied between chromosomes and taxonomic comparisons. Qualitatively, the patterns we observed in the empirical data and in our simulations suggest that selection drives rapid genome-wide transitions to multi-locus coupling, illustrating how divergence and gene flow interact along the speciation continuum. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Open AccessArticle Genomic Differentiation during Speciation-with-Gene-Flow: Comparing Geographic and Host-Related Variation in Divergent Life History Adaptation in Rhagoletis pomonella
Received: 25 February 2018 / Revised: 9 May 2018 / Accepted: 9 May 2018 / Published: 18 May 2018
PDF Full-text (1870 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
A major goal of evolutionary biology is to understand how variation within populations gets partitioned into differences between reproductively isolated species. Here, we examine the degree to which diapause life history timing, a critical adaptation promoting population divergence, explains geographic and host-related genetic
[...] Read more.
A major goal of evolutionary biology is to understand how variation within populations gets partitioned into differences between reproductively isolated species. Here, we examine the degree to which diapause life history timing, a critical adaptation promoting population divergence, explains geographic and host-related genetic variation in ancestral hawthorn and recently derived apple-infesting races of Rhagoletis pomonella. Our strategy involved combining experiments on two different aspects of diapause (initial diapause intensity and adult eclosion time) with a geographic survey of genomic variation across four sites where apple and hawthorn flies co-occur from north to south in the Midwestern USA. The results demonstrated that the majority of the genome showing significant geographic and host-related variation can be accounted for by initial diapause intensity and eclosion time. Local genomic differences between sympatric apple and hawthorn flies were subsumed within broader geographic clines; allele frequency differences within the races across the Midwest were two to three-fold greater than those between the races in sympatry. As a result, sympatric apple and hawthorn populations displayed more limited genomic clustering compared to geographic populations within the races. The findings suggest that with reduced gene flow and increased selection on diapause equivalent to that seen between geographic sites, the host races may be recognized as different genotypic entities in sympatry, and perhaps species, a hypothesis requiring future genomic analysis of related sibling species to R. pomonella to test. Our findings concerning the way selection and geography interplay could be of broad significance for many cases of earlier stages of divergence-with-gene flow, including (1) where only modest increases in geographic isolation and the strength of selection may greatly impact genetic coupling and (2) the dynamics of how spatial and temporal standing variation is extracted by selection to generate differences between new and discrete units of biodiversity. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Open AccessArticle Female Choice Undermines the Emergence of Strong Sexual Isolation between Locally Adapted Populations of Atlantic Mollies (Poecilia mexicana)
Received: 24 January 2018 / Revised: 23 April 2018 / Accepted: 25 April 2018 / Published: 2 May 2018
PDF Full-text (4927 KB) | HTML Full-text | XML Full-text
Abstract
Divergent selection between ecologically dissimilar habitats promotes local adaptation, which can lead to reproductive isolation (RI). Populations in the Poecilia mexicana species complex have independently adapted to toxic hydrogen sulfide and show varying degrees of RI. Here, we examined the variation in the
[...] Read more.
Divergent selection between ecologically dissimilar habitats promotes local adaptation, which can lead to reproductive isolation (RI). Populations in the Poecilia mexicana species complex have independently adapted to toxic hydrogen sulfide and show varying degrees of RI. Here, we examined the variation in the mate choice component of prezygotic RI. Mate choice tests across drainages (with stimulus males from another drainage) suggest that specific features of the males coupled with a general female preference for yellow color patterns explain the observed variation. Analyses of male body coloration identified the intensity of yellow fin coloration as a strong candidate to explain this pattern, and common-garden rearing suggested heritable population differences. Male sexual ornamentation apparently evolved differently across sulfide-adapted populations, for example because of differences in natural counterselection via predation. The ubiquitous preference for yellow color ornaments in poeciliid females likely undermines the emergence of strong RI, as female discrimination in favor of own males becomes weaker when yellow fin coloration in the respective sulfide ecotype increases. Our study illustrates the complexity of the (partly non-parallel) pathways to divergence among replicated ecological gradients. We suggest that future work should identify the genomic loci involved in the pattern reported here, making use of the increasing genomic and transcriptomic datasets available for our study system. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Open AccessArticle Chromosome Synapsis and Recombination in Male-Sterile and Female-Fertile Interspecies Hybrids of the Dwarf Hamsters (Phodopus, Cricetidae)
Received: 27 February 2018 / Revised: 9 April 2018 / Accepted: 18 April 2018 / Published: 25 April 2018
PDF Full-text (3900 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
Hybrid sterility is an important step in the speciation process. Hybrids between dwarf hamsters Phodopus sungorus and P. campbelli provide a good model for studies in cytological and genetic mechanisms of hybrid sterility. Previous studies in hybrids detected multiple abnormalities of spermatogenesis and
[...] Read more.
Hybrid sterility is an important step in the speciation process. Hybrids between dwarf hamsters Phodopus sungorus and P. campbelli provide a good model for studies in cytological and genetic mechanisms of hybrid sterility. Previous studies in hybrids detected multiple abnormalities of spermatogenesis and a high frequency of dissociation between the X and Y chromosomes at the meiotic prophase. In this study, we found that the autosomes of the hybrid males and females underwent paring and recombination as normally as their parental forms did. The male hybrids showed a significantly higher frequency of asynapsis and recombination failure between the heterochromatic arms of the X and Y chromosomes than the males of the parental species. Female hybrids as well as the females of the parental species demonstrated a high incidence of centromere misalignment at the XX bivalent and partial asynapsis of the ends of its heterochromatic arms. In all three karyotypes, recombination was completely suppressed in the heterochromatic arm of the X chromosome, where the pseudoautosomal region is located. We propose that this recombination pattern speeds up divergence of the X- and Y-linked pseudoautosomal regions between the parental species and results in their incompatibility in the male hybrids. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Graphical abstract

Open AccessArticle The Effects on Parapatric Divergence of Linkage between Preference and Trait Loci versus Pleiotropy
Received: 16 February 2018 / Revised: 2 April 2018 / Accepted: 6 April 2018 / Published: 17 April 2018
PDF Full-text (6742 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
Attempts to uncover the genetic basis of female mating preferences and male signals involved in reproductive isolation have discovered intriguing cases in which loci contributing to these traits co-localize in their chromosomal positions. Such discoveries raise the question of whether alleles at certain
[...] Read more.
Attempts to uncover the genetic basis of female mating preferences and male signals involved in reproductive isolation have discovered intriguing cases in which loci contributing to these traits co-localize in their chromosomal positions. Such discoveries raise the question of whether alleles at certain loci contribute pleiotropically to male and female components of premating reproductive isolation, versus whether these loci are merely tightly linked. Here we use population genetic models to assess the degree to which these alternatives affect both short term and equilibrium patterns of trait (signal) and preference divergence. We take advantage of the fact that in the case of secondary contact between populations exchanging migrants, patterns of divergence across the range of preference strengths differ markedly when preferences and traits are controlled by the same locus (the case of phenotype matching) versus when they are on separate chromosomes. We find that tight linkage between preference and trait loci can mimic the pleiotropic pattern for many generations (roughly the reciprocal of the recombination rate), but that any recombination ultimately results in equilibrium patterns of divergence far more similar to those found when preferences and traits are on separate chromosomes. In general, our finding that pleiotropy results in quite different long-term patterns from tight linkage highlights the importance of distinguishing between these possibilities in empirical systems. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Open AccessFeature PaperArticle Non-Pleiotropic Coupling of Daily and Seasonal Temporal Isolation in the European Corn Borer
Received: 30 January 2018 / Revised: 15 March 2018 / Accepted: 20 March 2018 / Published: 26 March 2018
PDF Full-text (3408 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
Speciation often involves the coupling of multiple isolating barriers to produce reproductive isolation, but how coupling is generated among different premating barriers is unknown. We measure the degree of coupling between the daily mating time and seasonal mating time between strains of European
[...] Read more.
Speciation often involves the coupling of multiple isolating barriers to produce reproductive isolation, but how coupling is generated among different premating barriers is unknown. We measure the degree of coupling between the daily mating time and seasonal mating time between strains of European corn borer (Ostrinia nubilalis) and evaluate the hypothesis that the coupling of different forms of allochrony is due to a shared genetic architecture, involving genes with pleiotropic effects on both timing phenotypes. We measure differences in gene expression at peak mating times and compare these genes to previously identified candidates that are associated with changes in seasonal mating time between the corn borer strains. We find that the E strain, which mates earlier in the season, also mates 2.7 h earlier in the night than the Z strain. Earlier daily mating is correlated with the differences in expression of the circadian clock genes cycle, slimb, and vrille. However, different circadian clock genes associate with daily and seasonal timing, suggesting that the coupling of timing traits is maintained by natural selection rather than pleiotropy. Juvenile hormone gene expression was associated with both types of timing, suggesting that circadian genes activate common downstream modules that may impose constraint on future evolution of these traits. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Graphical abstract

Open AccessArticle Evolutionary Mechanisms of Varying Chromosome Numbers in the Radiation of Erebia Butterflies
Received: 31 December 2017 / Revised: 14 March 2018 / Accepted: 14 March 2018 / Published: 16 March 2018
PDF Full-text (1788 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
The evolution of intrinsic barriers to gene flow is a crucial step in the process of speciation. Chromosomal changes caused by fusion and fission events are one such barrier and are common in several groups of Lepidoptera. However, it remains unclear if and
[...] Read more.
The evolution of intrinsic barriers to gene flow is a crucial step in the process of speciation. Chromosomal changes caused by fusion and fission events are one such barrier and are common in several groups of Lepidoptera. However, it remains unclear if and how chromosomal changes have contributed to speciation in this group. I tested for a phylogenetic signal of varying chromosome numbers in Erebia butterflies by combining existing sequence data with karyological information. I also compared different models of trait evolution in order to infer the underlying evolutionary mechanisms. Overall, I found significant phylogenetic signals that are consistent with non-neutral trait evolution only when parts of the mitochondrial genome were included, suggesting cytonuclear discordances. The adaptive evolutionary model tested in this study consistently outperformed the neutral model of trait evolution. Taken together, these results suggest that, unlike other Lepidoptera groups, changes in chromosome numbers may have played a role in the diversification of Erebia butterflies. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Review

Jump to: Research, Other

Open AccessReview The Role of Transposable Elements in Speciation
Received: 30 January 2018 / Revised: 26 April 2018 / Accepted: 26 April 2018 / Published: 15 May 2018
PDF Full-text (1077 KB) | HTML Full-text | XML Full-text
Abstract
Understanding the phenotypic and molecular mechanisms that contribute to genetic diversity between and within species is fundamental in studying the evolution of species. In particular, identifying the interspecific differences that lead to the reduction or even cessation of gene flow between nascent species
[...] Read more.
Understanding the phenotypic and molecular mechanisms that contribute to genetic diversity between and within species is fundamental in studying the evolution of species. In particular, identifying the interspecific differences that lead to the reduction or even cessation of gene flow between nascent species is one of the main goals of speciation genetic research. Transposable elements (TEs) are DNA sequences with the ability to move within genomes. TEs are ubiquitous throughout eukaryotic genomes and have been shown to alter regulatory networks, gene expression, and to rearrange genomes as a result of their transposition. However, no systematic effort has evaluated the role of TEs in speciation. We compiled the evidence for TEs as potential causes of reproductive isolation across a diversity of taxa. We find that TEs are often associated with hybrid defects that might preclude the fusion between species, but that the involvement of TEs in other barriers to gene flow different from postzygotic isolation is still relatively unknown. Finally, we list a series of guides and research avenues to disentangle the effects of TEs on the origin of new species. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Open AccessReview Genomic Signatures of Reinforcement
Received: 8 February 2018 / Revised: 27 March 2018 / Accepted: 28 March 2018 / Published: 3 April 2018
PDF Full-text (4620 KB) | HTML Full-text | XML Full-text
Abstract
Reinforcement is the process by which selection against hybridization increases reproductive isolation between taxa. Much research has focused on demonstrating the existence of reinforcement, yet relatively little is known about the genetic basis of reinforcement or the evolutionary conditions under which reinforcement can
[...] Read more.
Reinforcement is the process by which selection against hybridization increases reproductive isolation between taxa. Much research has focused on demonstrating the existence of reinforcement, yet relatively little is known about the genetic basis of reinforcement or the evolutionary conditions under which reinforcement can occur. Inspired by reinforcement’s characteristic phenotypic pattern of reproductive trait divergence in sympatry but not in allopatry, we discuss whether reinforcement also leaves a distinct genomic pattern. First, we describe three patterns of genetic variation we expect as a consequence of reinforcement. Then, we discuss a set of alternative processes and complicating factors that may make the identification of reinforcement at the genomic level difficult. Finally, we consider how genomic analyses can be leveraged to inform if and to what extent reinforcement evolved in the face of gene flow between sympatric lineages and between allopatric and sympatric populations of the same lineage. Our major goals are to understand if genome scans for particular patterns of genetic variation could identify reinforcement, isolate the genetic basis of reinforcement, or infer the conditions under which reinforcement evolved. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Other

Jump to: Research, Review

Open AccessPerspective Varied Genomic Responses to Maladaptive Gene Flow and Their Evidence
Received: 5 March 2018 / Revised: 17 May 2018 / Accepted: 30 May 2018 / Published: 13 June 2018
PDF Full-text (1897 KB) | HTML Full-text | XML Full-text | Supplementary Files
Abstract
Adaptation to a local environment often occurs in the face of maladaptive gene flow. In this perspective, I discuss several ideas on how a genome may respond to maladaptive gene flow during adaptation. On the one hand, selection can build clusters of locally
[...] Read more.
Adaptation to a local environment often occurs in the face of maladaptive gene flow. In this perspective, I discuss several ideas on how a genome may respond to maladaptive gene flow during adaptation. On the one hand, selection can build clusters of locally adaptive alleles at fortuitously co-localized loci within a genome, thereby facilitating local adaptation with gene flow (‘allele-only clustering’). On the other hand, the selective pressure to link adaptive alleles may drive co-localization of the actual loci relevant for local adaptation within a genome through structural genome changes or an evolving intra-genomic crossover rate (‘locus clustering’). While the expected outcome is, in both cases, a higher frequency of locally adaptive alleles in some genome regions than others, the molecular units evolving in response to gene flow differ (i.e., alleles versus loci). I argue that, although making this distinction is important, we commonly lack the critical empirical evidence to do so. This is mainly because many current approaches are biased towards detecting local adaptation in genome regions with low crossover rates. The importance of low-crossover genome regions for adaptation with gene flow, such as in co-localizing relevant loci within a genome, thus remains unclear. Future empirical investigations should address these questions by making use of comparative genomics, where multiple de novo genome assemblies from species evolved under different degrees of genetic exchange are compared. This research promises to advance our understanding of how a genome adapts to maladaptive gene flow, thereby promoting adaptive divergence and reproductive isolation. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Reproductive Isolation)
Figures

Figure 1

Back to Top