Roger K Butlin

The University of Sheffield | Sheffield · Department of Animal and Plant Sciences

Inversions are structural mutations that reverse the sequence of a chromosome segment and reduce the effective rate of recombination in the heterozygous state. They play a major role in adaptation, as well as in other evolutionary processes such as spe-ciation. Although inversions have been studied since the 1920s, they remain difficult to investig...

Inversions are thought to play a key role in adaptation and speciation, suppressing recombination between diverging populations. Genes influencing adaptive traits cluster in inversions, and changes in inversion frequencies are associated with environmental differences. However, in many organisms, it is unclear if inversions are geographically and t...

Predicting the outcomes of adaptation is a major goal of evolutionary biology. When temporal changes in the environment mirror spatial gradients, it opens up the potential for predicting the course of adaptive evolution over time based on patterns of spatial genetic and phenotypic variation. We assessed this approach in a 30-year transplant experim...

Speciation typically occurs in a time frame too long to be observed directly. This issue can be over-come by studying pairs of populations at different points in the speciation continuum, ideally within clades so that patterns are not confounded by differences among taxa. Such comparisons are possible in the marine snail Littorina saxatilis because...

Chromosomal rearrangements lead to the coupling of reproductive barriers, but whether and how they contribute to completion of speciation remains unclear. Marine snails of the genus Littorina repeatedly form hybrid zones between taxa segregating for inversion arrangements, providing opportunities to study this question. Here, we analysed two adjace...

Parallel evolution of phenotypic divergence offers compelling evidence supporting the influence of natural selection on the divergence process. However, the existence of ecotypes adapted to different habitats in separate locations is not a definitive proof of parallel evolution. Here, we leverage a large pool-seq dataset of the rocky-shore gastropo...

A growing body of research shows that chromosomal inversions, where each arrangement is associated with a certain environment and maintains a set of adaptive alleles, make an important contribution to local adaptation. However, inversions often remain unexplored across large geographical scales. It is unclear whether inversions contribute to adapta...

Understanding the factors that have shaped the current distributions and diversity of species is a central and longstanding aim of evolutionary biology. The recent inclusion of genomic data into phylogeographic studies has dramatically improved our understanding in organisms where evolutionary relationships have been challenging to infer. We used w...

Next-generation sequencing of pooled samples (Pool-seq) is a popular method to assess genome-wide diversity patterns in natural and experimental populations. However, Pool-seq is associated with specific sources of noise, such as unequal individual contributions. Consequently, using Pool-seq for the reconstruction of evolutionary history has remain...

Sandy beaches are biogeochemical hotspots that bridge marine and terrestrial ecosystems via the transfer of organic matter, such as seaweed (termed wrack). A keystone of this unique ecosystem is the microbial community, which helps to degrade wrack and re-mineralize nutrients. However, little is known about this community. Here, we characterize the...

Abstract: Key innovations are fundamental to biological diversification, but their genetic architecture is poorly understood. A recent transition from egg-laying to live-bearing in Littorina snails provides the opportunity to study the architecture of a young innovation. Samples do not cluster by reproductive mode in a genome-wide phylogeny, but lo...

Next-generation sequencing of pooled samples (Pool-seq) is an important tool in population genomics and molecular ecology. In Pool-seq, the relative number of reads with an allele reflects the allele frequencies in the sample. However, unequal individual contributions to the pool and sequencing errors can lead to inaccurate allele frequency estimat...

Next-generation sequencing of pooled samples (Pool-seq) is a popular method to assess genome-wide diversity patterns in natural and experimental populations. However, Pool-seq is associated with specific sources of noise, such as unequal individual contributions. Consequently, using Pool-seq for the reconstruction of evolutionary history has remain...

Chromosomal inversions have been shown to play a major role in local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better...

Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex‐determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex‐determining region. Chromosomal inversions may contribute to recom...

Supplementary materials of the article "The rise and fall of an alien: why the successful colonizer Littorina saxatilis failed to invade the Mediterranean Sea"

Understanding population divergence that eventually leads to speciation is essential for evolutionary biology. High species diversity in the sea was regarded as a paradox when strict allopatry was considered necessary for most speciation events because geographical barriers seemed largely absent in the sea, and many marine species have high dispers...

Understanding the genetic targets of natural selection is one of the most challenging goals of population genetics. Some of the earliest candidate genes were identified from associations between allozyme allele frequencies and environmental variation. One such example is the clinal polymorphism in the arginine kinase (Ak) gene in the marine snail L...

Local adaptation leads to differences between populations within a species. In many systems, similar environmental contrasts occur repeatedly, sometimes driving parallel phenotypic evolution. Understanding the genomic basis of local adaptation and parallel evolution is a major goal of evolutionary genomics. It is now known that by preventing the br...

Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutation accumulation can stabilize the system through...

Understanding what determines range expansion or extinction is crucial to predict the success of biological invaders. We tackled this long-standing question from an unparalleled perspective using the failed expansions in Littorina saxatilis and investigated its present and past habitat suitability in Europe through Ecological Niche Modelling. This...

Parasites have evolved proteins, virulence factors (VFs), that facilitate plant colonisation, however VFs mediating parasitic plant–host interactions are poorly understood. Striga hermonthica is an obligate, root‐parasitic plant of cereal hosts in sub‐Saharan Africa, causing devastating yield losses. Understanding the molecular nature and allelic v...

Hybridisation is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridisation has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridisation between sexual species within a genus or the typical...

Polymorphic short insertions and deletions (INDELs ≤ 50 bp) are abundant, although less common than single nucleotide polymorphisms (SNPs). Evidence from model organisms shows INDELs to be more strongly influenced by purifying selection than SNPs. Partly for this reason, INDELs are rarely used as markers for demographic processes or to detect balan...

Understanding where, when and how species’ ranges will be modified is both a fundamental problem and essential to predicting how spatio-temporal environmental changes in abiotic and biotic factors impact biodiversity. Notably, different species may respond disparately to similar environmental changes: some species may overcome an environmental chan...

Local adaptation is a fundamental evolutionary process generating biological diversity and potentially enabling ecological speciation. Divergent selection underlies the evolution of local adaptation in spatially structured populations by driving their adaptation toward local optima. Environments rarely differ along just one environmental axis; ther...

Understanding what determines range expansion or extinction is crucial to predict the success of biological invaders and effectively deal with biodiversity changes. We tackled this long-standing question from an unparalleled perspective using the failed expansions in Littorina saxatilis and investigating its present and past habitat suitability in...

Supergenes offer some of the most spectacular examples of long-term balancing selection in nature but their origin and maintenance remain a mystery. A critical aspect of supergenes is reduced recombination between arrangements. Reduced recombination protects adaptive multi-trait phenotypes, but can also lead to degeneration through mutation accumul...

Isolating mechanisms are characteristics of species that reduce or prevent successful reproduction with members of other species. Viewed genetically, they are characters that act as barriers to the exchange of genes between populations. Most of these barriers are incidental consequences of evolutionary processes within populations, but they can be...

Inversions often underlie complex adaptive traits, but the genic targets inside them are largely unknown. Gene expression profiling provides a powerful way to link inversions with their phenotypic consequences. We examined the effects of the Cf‐Inv(1) inversion in the seaweed fly Coelopa frigida on gene expression variation across sexes and life st...

Divergent selection applied to one or more traits drives local adaptation and may lead to ecological speciation. Divergent selection on many traits might be termed ‘multidimensional’ divergent selection. There is a commonly held view that multidimensional divergent selection is likely to promote local adaptation and speciation to a greater extent t...

Inversions often underlie complex adaptive traits, but the genic targets inside them are largely unknown. Gene expression profiling provides a powerful way to link inversions with their phenotypic consequences. We examined the effects of the Cf-Inv(1) inversion in the seaweed fly Coelopa frigida on gene expression variation across sexes and life st...

Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance for local adaptation we need to know their influence on pheno...

If there are no constraints on the process of speciation, then the number of species might be expected to match the number of available niches and this number might be indefinitely large. One possible constraint is the opportunity for allopatric divergence. In 1981, Felsenstein used a simple and elegant model to ask if there might also be genetic c...

Chromosomal inversions contribute widely to adaptation and speciation, yet they present a unique evolutionary puzzle as both their allelic content and frequency evolve in a feedback loop. In this simulation study, we quantified the role of the allelic content in determining the long-term fate of the inversion. Recessive deleterious mutations accumu...

Combining hybrid zone analysis with genomic data is a promising approach to understanding the genomic basis of adaptive divergence. It allows for the identification of genomic regions underlying barriers to gene flow. It also provides insights into spatial patterns of allele frequency change, informing about the interplay between environmental fact...

Speciation underlies the generation of novel biodiversity. Yet, there is much to learn about how natural selection shapes genomes during speciation. Selection is assumed to act against gene flow at barrier loci, promoting reproductive isolation. However, evidence for gene flow and selection is often indirect and we know very little about the tempor...

Speciation, that is, the evolution of reproductive barriers eventually leading to complete isolation, is a crucial process generating biodiversity. Recent work has contributed much to our understanding of how reproductive barriers begin to evolve, and how they are maintained in the face of gene flow. However, little is known about the transition fr...

The evolution of strong reproductive isolation (RI) is fundamental to the origins and maintenance of biological diversity, especially in situations where geographical distributions of taxa broadly overlap. But what is the history behind strong barriers currently acting in sympatry? Using whole-genome sequencing and single nucleotide polymorphism ge...

Zones of secondary contact between closely related taxa are a common legacy of the Quaternary ice ages. Despite their abundance, the factors that keep species apart and prevent hybridisation are often unknown. Here we study a very narrow contact zone between three closely related butterfly species of the Erebia tyndarus species complex. Using genom...

Inversions are chromosomal rearrangements where the order of genes is reversed. Inversions originate by mutation and can be under positive, negative or balancing selection. Selective effects result from potential disruptive effects on meiosis, gene disruption at inversion breakpoints and, importantly, the effects of inversions as modifiers of recom...

When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple‐eff...

The flat periwinkles, Littorina fabalis and L. obtusata, comprise two sister gastropod species that have an enormous potential to elucidate the mechanisms involved in ecological speciation in the marine realm. However, the molecular resources currently available for these species are still scarce. In order to circumvent this limitation, we used RNA...

The growth of snail shells can be described by simple mathematical rules. Variation in a few parameters can explain much of the diversity of shell shapes seen in nature. However, empirical studies of gastropod shell shape variation typically use geometric morphometric approaches, which do not capture this growth pattern. We have developed a way to...

When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple-eff...

Abstract Characterizing the patterns of hybridization between closely related species is crucial to understand the role of gene flow in speciation. In particular, systems comprising multiple contacts between sister species offer an outstanding opportunity to investigate how reproductive isolation varies with environmental conditions, demography and...

The study of parallel ecological divergence provides important clues to the operation of natural selection. Parallel divergence often occurs in heterogeneous environments with different kinds of environmental gradients in different locations, but the genomic basis underlying this process is unknown. We investigated the genomics of rapid parallel ad...

Genetic incompatibilities contribute to reproductive isolation between many diverging populations, but it is still unclear to what extent they play a role if divergence happens with gene flow. In contact zones between the "Crab" and "Wave" ecotypes of the snail Littorina saxatilis divergent selection forms strong barriers to gene flow, while the ro...

The idea that populations must be geographically isolated (allopatric) to evolve into separate species has persisted for a long time. It is now clear that new species can also diverge despite ongoing genetic exchange, but few accepted cases of speciation in sympatry have held up when scrutinised using modern approaches. Here, we examined evidence f...

Although it is now widely accepted that speciation can occur in the face of continuous gene flow, with little or no spatial separation, the mechanisms and genomic architectures that permit such divergence are still debated. Here, we examined speciation in the face of gene flow in the Howea palms of Lord Howe Island, Australia. We built a genetic ma...

Population genetic models of evolution along linear ecological gradients cannot explain why adaptation stops at ecological margins. This is because, unless models impose reductions in carrying capacity at species’ edges, the dominant effect of gene flow is to increase genetic variance and adaptive potential rather than swamping local adaptation. Th...

Newts of the genus Triturus (marbled and crested newts) exhibit substantial variation in the number of trunk vertebrae (NTV) and a higher NTV corresponds to a longer annual aquatic period. Because the Triturus phylogeny has thwarted resolution to date, the evolutionary history of NTV, annual aquatic period, and their potential coevolution has remai...

Empirical data suggest that inversions in many species contain genes important for intraspecific divergence and speciation, yet mechanisms of evolution remain unclear. While genes inside an inversion are tightly linked, inversions are not static but evolve separately from the rest of the genome by new mutations, recombination within arrangements, a...

Hybrid zone movement may result in substantial unidirectional introgression of selectively neutral material from the local to the advancing species, leaving a genetic footprint. This genetic footprint is represented by a trail of asymmetric tails and displaced cline centres in the wake of the moving hybrid zone. A peak of admixture linkage disequil...

The current aim of speciation research is to pin-point which genomic regions serve as barriers for gene flow and drive divergence during speciation. At the barrier loci, natural selection is assumed to act against gene flow. Many current approaches, however, rely on indirect measures of gene flow and natural selection. Here we present a system to t...

Both classical and recent studies suggest that chromosomal inversion polymorphisms are important in adaptation and speciation. However, biases in discovery and reporting of inversions make it difficult to assess their prevalence and biological importance. Here, we use an approach based on linkage disequilibrium among markers genotyped for samples c...

Understanding the course of eco-morphological evolution in adaptive radiations is challenging as the phylogenetic relationships among the species involved are typically difficult to resolve. Newts of the genus Triturus (marbled and crested newts) are a well-studied case: they exhibit substantial variation in the number of trunk vertebrae (NTV) and...

The genetic basis of parallel ecological divergence provides important clues to the operation of natural selection and the predictability of evolution. Many examples exist where binary environmental contrasts seem to drive parallel divergence. However, this simplified view can conceal important components of parallel divergence because environmenta...

The evolution of assortative mating is a key part of the speciation process. Stronger assortment, or greater divergence in mating traits, between species pairs with overlapping ranges is commonly observed, but possible causes of this pattern of reproductive character displacement are difficult to distinguish. We use a multidisciplinary approach to...

Figure S6. Posterior distributions of the NM model parameters.

Table S1. Collection sites of Littoraria cingulata and L. filosa. Table S2. Analysis of individual penis traits (after size correction). Table S3. Uniform prior distributions [low bound – high bound], after having ensured that priors included the posteriors. Table S4. Parameter estimation under the NM model, chosen for having received the highes...

Figure S4. Posterior probabilities of models NM and RM over 100 rounds of leave‐one‐out cross‐validation analysis.

Figure S1. Feature extraction from penis drawings (see Supplementary Methods for details).

Figure S2. Demographic models investigated in this study.

Figure S3. Trajectory analysis of penis form.