Biology subjects

Butlin, R. K.

Publications and source records attributed to Butlin, R. K..

17 recordsLinked to original sources

bioRxiv2026

The role of chromosomal inversions in local adaptation and ecotype formation across a variable landscape in an intertidal snail

Adaption to environmental variation can be discrete or continuous, responding to sharp or gradual habitat transitions. Chromosomal inversions accentuate these adaptive responses as multiple loci respond in tandem across a habitat transition. Earlier studies of Littorina saxatilis (Olivi, 1792) have shown that three ecotypes segregate in different habitats supported by polymorphisms in a few inversions. However, many more large inversions are polymorphic in this species and potentially have adaptive effects in response to uncharacterised environmental gradients. We sampled 200 random shores representing all kinds of shore habitats present in a 12x12 km area of a Swedish archipelago, with L. saxatilis found at 196 sites. Environment and shell morphology were summarised using dimension reduction analyses, and Bayesian regression models were used to analyse the relationships between phenotype, environment and inversions. Phenotypic variation was a continuum with previously described ecotypes positioned in different parts. 18 inversions responded to at least one dimension of environmental variation, and over (12) half influenced the measured phenotypes. Overall, inversion arrangements explained 15% of phenotypic variation, with limited direct contributions from the environment (<1%). Chromosomal inversions thus are a major factor for local adaptation in L. saxatilis, supporting adaptation across a landscape more complex than the previously described ecotypes.

evolutionary biology↗

bioRxiv2024

Chromosome-scale genome assembly of the rough periwinkle Littorina saxatilis

The intertidal gastropod Littorina saxatilis is a model system to study speciation and local adaptation. The repeated occurrence of distinct ecotypes showing different levels of genetic divergence makes L. saxatilis particularly suited to study different stages of the speciation continuum in the same lineage. A major finding is the presence of several large chromosomal inversions associated with the divergence of ecotypes and, specifically, the species offers a system to study the role of inversions in this divergence. The genome of L. saxatilis is 1.35Gb and composed of 17 chromosomes. The first reference genome of the species was assembled using Illumina data, was highly fragmented (N50 of 44kb) and was quite incomplete, with a BUSCO completeness of 80.1% on the Metazoan dataset. A linkage map of one full-sibling family enabled the placement of 587 Mbp of the genome into 17 linkage groups corresponding to the haploid number of chromosomes, but the fragmented nature of this reference genome limited the understanding of the interplay between divergent selection and gene flow during ecotype formation. Here we present a newly generated reference genome that is highly contiguous, with a N50 of 67 Mb and 90.4% of the total assembly length placed in 17 super-scaffolds. It is also highly complete with a BUSCO completeness of 94.1 % of the Metazoa dataset. This new reference will allow for investigations into the genomic regions implicated in ecotype formation as well as better characterization of the inversions and their role in speciation. SignificanceThe rough periwinkle, L. saxatilis has become a model to study adaptation, evolutionary innovation and speciation, including the role of chromosomal inversions in these processes. Chromosomal inversions have also been identified in other species of Littorina providing a valuable opportunity for investigating their origin and evolution. Here, we present a new chromosome-scale reference genome of L. saxatilis generated from long reads and HiC chromatin proximity mapping replacing an earlier highly fragmented genome. This will enable detailed investigations of how inversions contribute to adaptation and reproductive isolation in L. saxatilis and related taxa, including studies of the effects of individual loci within and outside inversions.

genomics↗

bioRxiv2023

Predicting rapid adaptation in time from adaptation in space: a 30-year field experiment in marine snails

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 experiment in the marine snail Littorina saxatilis. In 1992, snails were transplanted from a predation-dominated environment to one dominated by wave action. Based on spatial patterns, we predicted transitions in shell size and morphology, allele frequencies at positions throughout the genome, and chromosomal rearrangement frequencies. Observed changes closely agreed with predictions. Hence, transformation can be both dramatic and rapid, and predicted from knowledge of the phenotypic and genetic variation among populations.

evolutionary biology↗

bioRxiv2023

Phenotypic divergence and genomic architecture at two different stages of speciation in a marine snail

Speciation typically occurs over too long a time frame to be observed directly. A way forward is to compare pairs of ecotypes that evolved in parallel in similar contexts but have reached different degrees of reproductive isolation. Such comparisons are possible in the marine snail Littorina saxatilis by contrasting barriers to gene flow between parallel ecotypes in Spain and Sweden. In both countries, divergent ecotypes have evolved to withstand either crab predation or wave action. Here, we explore transects spanning contact zones between the Crab and the Wave ecotypes using low-coverage whole-genome sequencing, morphological and behavioural traits. Despite parallel phenotypic divergence, distinct patterns of differentiation between the ecotypes emerged: a continuous cline in Sweden indicating a weak barrier to gene flow, but two highly genetically and phenotypically divergent, and partly spatially-overlapping clusters in Spain suggesting a much stronger barrier to gene flow. Absence of Spanish early-generation hybrids supported strong isolation, but a low level of gene flow is evident from molecular data. In both countries, highly differentiated loci were located in both shared and private chromosomal inversions but were also present in collinear regions. Despite being considered the same species and showing similar levels of phenotypic divergence, the Spanish ecotypes are much closer to full reproductive isolation than the Swedish ones. Barriers to gene flow of very different strengths between ecotypes within the same species might be explained by dissimilarities in the spatial arrangement of habitats, the selection gradients or the ages of the systems. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=158 SRC="FIGDIR/small/558824v2_ufig2.gif" ALT="Figure 2"> View larger version (38K): org.highwire.dtl.DTLVardef@c72ac4org.highwire.dtl.DTLVardef@1c8cd22org.highwire.dtl.DTLVardef@13ac83org.highwire.dtl.DTLVardef@1a301d6_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical abstract.C_FLOATNO Distinct patterns of divergence between parallel ecotypes in Sweden and Spain. C_FIG

evolutionary biology↗

bioRxiv2023

Parallel evolution of local adaptation in Littorina saxatilis inferred with whole-genome pool-seq data

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 gastropod, Littorina saxatilis to compare and contrast two explicit scenarios of ecotype formation. Populations of this species inhabit contrasting habitats, where the main selective pressure is either wave action or crab predation. Using approximate Bayesian computation to jointly infer demographic parameters and account for pool-seq specific sources of uncertainty, our analysis reveals that ecotype formation at a large geographical scale has occurred in parallel. Parameter estimates provide strong support for a demographic history marked by the spatial separation of the ancestral populations that later gave rise to parallel evolution of ecotypes in Spain and Sweden. Additionally, ecotype formation occurred in the face of continuous gene flow between the diverging ecotypes. These results shed new light on a important model of speciation driven by ecological factors and emphasize the effectiveness of combining pool-seq with ABC for studying parallel evolution across diverse geographical regions.

evolutionary biology↗

bioRxiv2023

Selection on many loci drove the origin and spread of a key innovation

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 an innovation that has evolved repeatedly in animals. Samples do not cluster by reproductive mode in a genome-wide phylogeny, but local genealogical analysis revealed numerous genomic regions where all live-bearers carry the same core haplotype. Associated regions show evidence for live-bearer-specific positive selection, and are enriched for genes that are differentially expressed between egg-laying and live-bearing reproductive systems. Ages of selective sweeps suggest live-bearing alleles accumulated gradually, involving selection at different times in the past. Our results suggest that innovation can have a polygenic basis, and that novel functions can evolve gradually, rather than in a single step.

evolutionary biology↗

bioRxiv2023

poolHelper: an R package to help in designing Pool-Seq studies

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 estimates. When designing Pool-seq studies, researchers need to decide the pool size (number of individuals) and average depth of coverage (sequencing effort). An efficient sampling design should maximize the accuracy of allele frequency estimates while minimizing the sequencing effort. We introduce an R package, poolHelper, enabling users to simulate Pool-seq data under different combinations of average depth of coverage, pool sizes and number of pools, accounting for unequal individual contribution and sequencing errors, modelled by parameters that users can modify. poolHelper can be used to assess how different combinations of those parameters influence the error of sample allele frequencies and expected heterozygosity. The mean absolute error is computed by comparing the sample allele frequencies obtained based on individual genotypes with the frequency estimates obtained with Pool-seq. Using simulations under a single population model, we illustrate that increasing the depth of coverage does not necessarily lead to more accurate estimates, reinforcing that finding the best Pool-seq study design is not straightforward. Moreover, we show that simulations can be used to identify different combinations of parameters with similarly low mean absolute errors. The poolHelper package provides tools for performing simulations with different combinations of parameters before sampling and generating data, allowing users to define sampling schemes that minimize the sequencing effort.

bioinformatics↗

bioRxiv2022

Identification of candidate virulence loci in Striga hermonthica, a devastating parasite of African cereal crops

O_LIParasites have evolved proteins, Virulence Factors (VFs), that facilitate plant colonization, yet 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 variation of VFs in S. hermonthica is essential for breeding resistance and delaying the evolution of parasite virulence. C_LIO_LIWe assembled the S. hermonthica genome and identified secreted proteins by in silico prediction. Pooled sequencing of parasites growing on a susceptible and a strongly resistant rice host allowed us to scan for loci where selection imposed by the resistant host had elevated the frequency of alleles contributing to successful colonisation. C_LIO_LIThirty-eight putatively secreted VFs had extremely different allele frequencies with functions including host cell wall modification, protease inhibitors, oxidoreductase and kinase activities. These candidate loci had significantly higher Tajimas D than the genomic background, consistent with balancing selection. C_LIO_LIOur results reveal diverse strategies used by S. hermonthica to overcome different layers of host resistance. Understanding the maintenance of variation at virulence loci by balancing selection will be critical to managing the evolution of virulence as a part of a sustainable control strategy. C_LI

plant biology↗

bioRxiv2021

Supergene degeneration opposes polymorphism: The curious case of balanced lethals

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 accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One such outcome is the formation of balanced lethal systems, a maladaptive system where both supergene arrangements have accumulated deleterious mutations to the extent that both homozygotes are inviable, leaving only heterozygotes to reproduce. Here, we perform a simulation study to understand the conditions under which these different outcomes occur, assuming a scenario of introgression after allopatric divergence. We found that AOD aids the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism is easily destabilized by further mutation accumulation. While degradation may strengthen AOD, thereby stabilizing the supergene polymorphism, it is often asymmetric, which is the key disrupter of the quasi-equilibrium state of the polymorphism. Furthermore, mechanisms that accelerate degeneration also tend to amplify asymmetric mutation accumulation between the supergene arrangements and vice versa. As the evolution of a balanced lethal system requires symmetric degradation of both arrangements, this leaves highly restricted conditions under which such a system could evolve. We show that small population size and low dominance coefficients are critical factors, as these reduce the efficacy of selection. The dichotomy between the persistence of a polymorphism and degradation of supergene arrangements likely underlies the rarity of balanced lethal systems in nature.

evolutionary biology↗

bioRxiv2021

A metagenomic analysis of the wrackbed microbiome indicates a phylogeographic break along the North Sea - Baltic Sea transition zone

Sandy beaches are biogeochemical hotspots that bridge marine and terrestrial ecosystems via the transfer of marine 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 the wrackbed microbiome, its composition, trophic ecology, or how it varies over time and space. Here we characterize the wrackbed microbiome as well as the microbiome of a primary consumer, the seaweed fly Coelopa frigida, and examine how they change along one of the most studied ecological gradients in the world, the transition from the marine North Sea to the brackish Baltic Sea. We found that polysaccharide degraders dominated both the wrackbed and seaweed fly microbiomes but there were still consistent differences between wrackbed and fly samples. Furthermore, we observed a shift in both microbial communities and functionality between the North and Baltic Sea. These shifts were mostly due to changes in the frequency of different groups of known polysaccharide degraders (Proteobacteria and Bacteroidota). We hypothesize that microbes were selected for their abilities to degrade different polysaccharides corresponding to a shift in polysaccharide content in the seaweed communities of the North vs. Baltic Sea. Our results reveal the complexities of both the wracked microbial community, with different groups specialized to different roles, and the cascading trophic consequences of shifts in the near shore algal community.

genomics↗

bioRxiv2021

A large chromosomal inversion shapes gene expression in seaweed flies (Coelopa frigida)

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 stages. Our analyses revealed that Cf-Inv(1) shapes global expression patterns but the extent of this effect is variable with much stronger effects in adults than larvae. Furthermore, within adults, both common as well as sex specific patterns were found. The vast majority of these differentially expressed genes mapped to Cf-Inv(1). However, genes that were differentially expressed in a single context (i.e. in males, females or larvae) were more likely to be located outside of Cf-Inv(1). By combining our findings with genomic scans for environmentally associated SNPs, we were able to pinpoint candidate variants in the inversion that may underlie mechanistic pathways that determine phenotypes. Together the results in this study, combined with previous findings, support the notion that the polymorphic Cf-Inv(1) inversion in this species is a major factor shaping both coding and regulatory variation resulting in highly complex adaptive effects.

evolutionary biology↗

bioRxiv2020

Assortative mating, sexual selection and their consequences for gene flow in Littorina

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-effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis, occur in North Atlantic rocky-shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size-assortative mating has previously been documented. Here, we analyze the mating pattern in L. saxatilis with respect to size in intensively-sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment.

evolutionary biology↗

bioRxiv2019

Muller’s Ratchet and the Long-Term Fate of Chromosomal Inversions

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 accumulated on both arrangements with most of them being private to a given arrangement. This led to increasing overdominance, allowing for the maintenance of the inversion polymorphism and generating strong non-adaptive divergence between arrangements. The accumulation of mutations was mitigated by gene conversion but nevertheless led to the fitness decline of at least one homokaryotype under all considered conditions. Surprisingly, this fitness degradation could be permanently halted by the branching of an arrangement into multiple highly divergent haplotypes. Our results highlight the dynamic features of inversions by showing how the non-adaptive evolution of allelic content can play a major role in the fate of the inversion. Author SummaryA chromosomal inversion is a segment of the chromosome that is flipped (inverted arrangement) relative to the normal orientation (standard arrangement). Such structural mutations may facilitate evolutionary processes such as adaptation and speciation, because reduced recombination in inverted regions allows beneficial combinations of alleles to behave as a "single unit". This locally reduced recombination can have major consequences for the evolution of the allelic content inside the inversion. We used simulations to investigate some of these consequences. Inverted regions tended to accumulate more deleterious recessive mutations than the rest of the genome, which decreased the fitness of homokarotypes (individuals with two copies of the same arrangement). This led to a strong selective advantage for heterokaryotypes (individuals with one copy of each arrangement), maintaining the inversion polymorphism in the population. The accumulation of deleterious mutations also resulted in strong divergence between arrangements. We occasionally observed an arrangement that diverged into a small number of highly differentiated haplotypes, stopping the fitness decrease in homokaryotypes. Our results highlight the dynamic features of inversions by showing how the evolution of allelic content can greatly affect the fate of an inversion.

evolutionary biology↗

bioRxiv2018

Hybridizing wood ants allow testing for natural selection at candidate barrier loci underlying speciation

While speciation underlies novel biodiversity, it is poorly understood how natural selection shapes genomes during speciation. Selection is assumed to act against gene flow at barrier loci, promoting reproductive isolation and speciation. However, evidence for gene flow and selection is often indirect. Here we utilize haplodiploidy to identify candidate barrier loci in hybrids between two wood ant species and integrate survival analysis to directly measure if natural selection is acting at candidate barrier loci. We find multiple candidate barrier loci but surprisingly, proportion of them show leakage between samples collected ten years apart, natural selection favoring leakage in the latest sample. Barrier leakage and natural selection for introgressed alleles could be due to environment-dependent selection, emphasizing the need to consider temporal variation in natural selection in future speciation work. Integrating data on survival allows us to move beyond genome scans, demonstrating natural selection acting on hybrid genomes in real-time.

evolutionary biology↗

bioRxiv2018

Phylogenomics of the adaptive radiation of Triturus newts supports gradual ecological niche expansion towards an incrementally aquatic lifestyle

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 remained unclear. To resolve the phylogeny of Triturus, we generated a c. 6,000 transcriptome-derived marker data set using a custom target enrichment probe set, and conducted phylogenetic analyses using: 1) data concatenation with RAxML, 2) gene-tree summary with ASTRAL, and 3) species-tree estimation with SNAPP. All analyses produce the same, highly supported topology, despite cladogenesis having occurred over a short timeframe, resulting in short internal branch lengths. Our new phylogenetic hypothesis is consistent with the minimal number of inferred changes in NTV count necessary to explain the diversity in NTV observed today. Although a causal relationship between NTV, body form, and aquatic ecology has yet to be experimentally established, our phylogeny indicates that these features have evolved together, and suggest that they may underlie the adaptive radiation that characterizes Triturus.

evolutionary biology↗

bioRxiv2018

Inter- and intra-specific genomic divergence in Drosophila montana shows evidence for cold adaptation

The genomes of species that are ecological specialists will likely contain signatures of genomic adaptation to their niche. However, distinguishing genes related to their ecological specialism from other sources of selection and more random changes is a challenge. Here we describe the genome of Drosophila montana, the most extremely cold-adapted Drosophila species. We describe the genome, which is similar in size and gene content to most Drosophila species. We look for evidence of accelerated divergence from a previously sequenced relative, and do not find strong evidence for divergent selection on coding sequence variation. We use branch tests to identify genes showing accelerated divergence in contrasts between cold- and warm adapted species and identify about 250 genes that show differences, possibly driven by a lower synonymous substitution rate in cold-adapted species. Divergent genes are involved in a variety of functions, including cuticular and olfactory processes. We also re-sequenced three populations of D. montana representing its ecological and geographic range. Outlier loci were more likely to be found on the X chromosome and there was a greater than expected overlap between population outliers and those genes implicated in cold adaptation between Drosophila species, implying some continuity of selective process at these different evolutionary scales.

genomics↗

bioRxiv2017

Conflict between heterozygote advantage and hybridincompatibility in haplodiploids (and sex chromosomes)

In many diploid species the sex chromosomes play a special role in mediating reproductive isolation. In haplodiploids, where females are diploid and males haploid, the whole genome behaves similarly to the X/Z chromosomes of diploids. Therefore, haplodiploid systems can serve as a model for the role of sex chromosomes in speciation and hybridization. A previously described population of Finnish Formica wood ants displays genome-wide signs of ploidally and sexually antagonistic selection resulting from hybridization. Here, hybrid females have increased survivorship but hybrid males are inviable. To understand how the unusual hybrid population may be maintained, we developed a mathematical model with hybrid incompatibility, female heterozygote advantage, recombination, and assortative mating. The rugged fitness landscape resulting from the co-occurrence of heterozygote advantage and hybrid incompatibility results in a sexual conflict in haplodiploids, which is caused by the ploidy difference. Thus, whereas heterozygote advantage always promotes long-term polymorphism in diploids, we find various outcomes in haplodiploids in which the population stabilizes either in favor of males, females, or via maximizing the number of introgressed individuals. We discuss these outcomes with respect to the potential long-term fate of the Finnish wood ant population, and provide approximations for the extension of the model to multiple incompatibilities. Moreover, we highlight the general implications of our results for speciation and hybridization in haplodiploids versus diploids, and how the described fitness relationships could contribute to the outstanding role of sex chromosomes as hotspots of sexual antagonism and genes involved in speciation.

evolutionary biology↗