Negative Coupling: The Coincidence of Premating Isolating Barriers Can Reduce Reproductive Isolation.

Speciation can be mediated by a variety of reproductive barriers, and the interaction among different barriers has often been shown to enhance overall reproductive isolation, a process referred to as "coupling." Here, we analyze a population genetics model to study the establishment of linkage disequilibrium (LD) among loci involved in multiple premating barriers, an aspect that has received little theoretical attention to date. We consider a simple genetic framework underlying two distinct premating barriers, each encoded by a preference locus and its associated mating trait locus. We show that their interaction can lead to a decrease in overall reproductive isolation relative to a situation with a single barrier, a process we call "negative coupling." More specifically, in our model, negative coupling results either from sexual selection that reduces divergence at all loci, or from reduced LD that occurs because the presence of many females with "mismatched" preferences causes the mating success of recombinant males to become high. Interestingly, the latter effect may even cause LD among preference loci to become negative when recombination rates among loci are low. We conclude that coincident reproductive barriers may not necessarily reinforce each other, and that the underlying loci may not necessarily develop a positive association.

Diverse pathways to speciation revealed by marine snails.

Speciation is a key evolutionary process that is not yet fully understood. Combining population genomic and ecological data from multiple diverging pairs of marine snails (Littorina) supports the search for speciation mechanisms. Placing pairs on a one-dimensional speciation continuum, from undifferentiated populations to species, obscured the complexity of speciation. Adding multiple axes helped to describe either speciation routes or reproductive isolation in the snails. Divergent ecological selection repeatedly generated barriers between ecotypes, but appeared less important in completing speciation while genetic incompatibilities played a key role. Chromosomal inversions contributed to genomic barriers, but with variable impact. A multidimensional (hypercube) approach supported framing of questions and identification of knowledge gaps and can be useful to understand speciation in many other systems.

How chromosomal inversions reorient the evolutionary process.

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 speciation. Although inversions have been studied since the 1920s, they remain difficult to investigate because the reduced recombination conferred by them strengthens the effects of drift and hitchhiking, which in turn can obscure signatures of selection. Nonetheless, numerous inversions have been found to be under selection. Given recent advances in population genetic theory and empirical study, here we review how different mechanisms of selection affect the evolution of inversions. A key difference between inversions and other mutations, such as single nucleotide variants, is that the fitness of an inversion may be affected by a larger number of frequently interacting processes. This considerably complicates the analysis of the causes underlying the evolution of inversions. We discuss the extent to which these mechanisms can be disentangled, and by which approach.

The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution.

Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life.

Clones on the run: The genomics of a recently expanded partially clonal species.

Why species that in their core areas mainly reproduce sexually become enriched with clones in marginal populations ("geographic parthenogenesis") remains unclear. Earlier hypotheses have emphasized that selection might promote clonality because it protects locally adapted genotypes. On the other hand, it also hampers recombination and adaptation to changing conditions. The aim of the present study was to investigate the early stages of range expansion in a partially clonal species and what drives an increase in cloning during such expansion. We used genome-wide sequencing to investigate the origin and evolution of large clones formed in a macroalgal species (Fucus vesiculosus) during a recent expansion into the postglacial Baltic Sea. We found low but persistent clonality in core populations, while at range margins, large dominant clonal lineages had evolved repeatedly from different sexual populations. A range expansion model showed that even when asexual recruitment is less favourable than sexual recruitment in core populations, repeated bottlenecks at the expansion front can establish a genetically eroded clonal wave that spreads ahead of a sexual wave into the new area. Genetic variation decreases by drift following repeated bottlenecks at the expansion front. This results in the emerging clones having low expected heterozygosity, which corroborated our empirical observations. We conclude that Baker's Law (clones being favoured by uniparental reproductive assurance in new areas) can play an important role during range expansion in partially clonal species, resulting in a complex spatiotemporal mosaic of clonal and sexual lineages that might persist during thousands of generations.

Ten years of marine evolutionary biology-Challenges and achievements of a multidisciplinary research initiative.

The Centre for Marine Evolutionary Biology (CeMEB) at the University of Gothenburg, Sweden, was established in 2008 through a 10-year research grant of 8.7 m€ to a team of senior researchers. Today, CeMEB members have contributed >500 scientific publications, 30 PhD theses and have organised 75 meetings and courses, including 18 three-day meetings and four conferences. What are the footprints of CeMEB, and how will the centre continue to play a national and international role as an important node of marine evolutionary research? In this perspective article, we first look back over the 10 years of CeMEB activities and briefly survey some of the many achievements of CeMEB. We furthermore compare the initial goals, as formulated in the grant application, with what has been achieved, and discuss challenges and milestones along the way. Finally, we bring forward some general lessons that can be learnt from a research funding of this type, and we also look ahead, discussing how CeMEB's achievements and lessons can be used as a springboard to the future of marine evolutionary biology.

Ten years of demographic modelling of divergence and speciation in the 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 dispersal capacities. Combining genome-wide data with demographic modelling to infer the demographic history of divergence has introduced new ways to address this classical issue. These models assume an ancestral population that splits into two subpopulations diverging according to different scenarios that allow tests for periods of gene flow. Models can also test for heterogeneities in population sizes and migration rates along the genome to account, respectively, for background selection and selection against introgressed ancestry. To investigate how barriers to gene flow arise in the sea, we compiled studies modelling the demographic history of divergence in marine organisms and extracted preferred demographic scenarios together with estimates of demographic parameters. These studies show that geographical barriers to gene flow do exist in the sea but that divergence can also occur without strict isolation. Heterogeneity of gene flow was detected in most population pairs suggesting the predominance of semipermeable barriers during divergence. We found a weak positive relationship between the fraction of the genome experiencing reduced gene flow and levels of genome-wide differentiation. Furthermore, we found that the upper bound of the 'grey zone of speciation' for our dataset extended beyond that found before, implying that gene flow between diverging taxa is possible at higher levels of divergence than previously thought. Finally, we list recommendations for further strengthening the use of demographic modelling in speciation research. These include a more balanced representation of taxa, more consistent and comprehensive modelling, clear reporting of results and simulation studies to rule out nonbiological explanations for general results.

A decade of progress in marine evolutionary biology.

This article summarizes the Evolutionary Applications Special Issue, "A decade of progress in Marine Evolutionary Biology." The globally connected ocean, from its pelagic depths to its highly varied coastlines, inspired Charles Darwin to develop the theory of evolution during the voyage of the Beagle. As technology has developed, there has been a dramatic increase in our knowledge about life on our blue planet. This Special Issue, composed of 19 original papers and seven reviews, represents a small contribution to the larger picture of recent research in evolutionary biology, and how such advancements come about through the connection of researchers, their fields, and their knowledge. The first European network for marine evolutionary biology, the Linnaeus Centre for Marine Evolutionary Biology (CeMEB), was developed to study evolutionary processes in the marine environment under global change. Though hosted by the University of Gothenburg in Sweden, the network quickly grew to encompass researchers throughout Europe and beyond. Today, more than a decade after its foundation, CeMEB's focus on the evolutionary consequences of global change is more relevant than ever, and knowledge gained from marine evolution research is urgently needed in management and conservation. This Special Issue, organized and developed through the CeMEB network, contains contributions from all over the world and provides a snapshot of the current state of the field, thus forming an important basis for future research directions.

Adaptive, maladaptive, neutral, or absent plasticity: Hidden caveats of reaction norms.

Adaptive phenotypic plasticity may improve the response of individuals when faced with new environmental conditions. Typically, empirical evidence for plasticity is based on phenotypic reaction norms obtained in reciprocal transplant experiments. In such experiments, individuals from their native environment are transplanted into a different environment, and a number of trait values, potentially implicated in individuals' response to the new environment, are measured. However, the interpretations of reaction norms may differ depending on the nature of the assessed traits, which may not be known beforehand. For example, for traits that contribute to local adaptation, adaptive plasticity implies nonzero slopes of reaction norms. By contrast, for traits that are correlated to fitness, high tolerance to different environments (possibly due to adaptive plasticity in traits that contribute to adaptation) may, instead, result in flat reaction norms. Here we investigate reaction norms for adaptive versus fitness-correlated traits and how they may affect the conclusions regarding the contribution of plasticity. To this end, we first simulate range expansion along an environmental gradient where plasticity evolves to different values locally and then perform reciprocal transplant experiments in silico. We show that reaction norms alone cannot inform us whether the assessed trait exhibits locally adaptive, maladaptive, neutral, or no plasticity, without any additional knowledge of the traits assessed and species' biology. We use the insights from the model to analyse and interpret empirical data from reciprocal transplant experiments involving the marine isopod Idotea balthica sampled from two geographical locations with different salinities, concluding that the low-salinity population likely has reduced adaptive plasticity relative to the high-salinity population. Overall, we conclude that, when interpreting results from reciprocal transplant experiments, it is necessary to consider whether traits assessed are locally adaptive with respect to the environmental variable accounted for in the experiments or correlated to fitness.

Introduction to the theme issue 'Species' ranges in the face of changing environments'.

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 change only with difficulty or not at all, while other species may readily overcome the same change. Ranges may contract, expand or move. The drivers and consequences of this variability in species' responses remain puzzling. Importantly, changes in a species' range creates feedbacks to the environmental conditions, populations and communities in its previous and current range, rendering population genetic, population dynamic and community processes inextricably linked. Understanding these links is critical in guiding biodiversity management and conservation efforts. This theme issue presents current thinking about the factors and mechanisms that limit and/or modify species' ranges. It also outlines different approaches to detect changes in species' distributions, and illustrates cases of range modifications in several taxa. Overall, this theme issue highlights the urgency of understanding species' ranges but shows that we are only just beginning to disentangle the processes involved. One way forward is to unite ecology with evolutionary biology and empirical with modelling approaches. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

The role of phenotypic plasticity in the establishment of range margins.

It has been argued that adaptive phenotypic plasticity may facilitate range expansions over spatially and temporally variable environments. However, plasticity may induce fitness costs. This may hinder the evolution of plasticity. Earlier modelling studies examined the role of plasticity during range expansions of populations with fixed genetic variance. However, genetic variance evolves in natural populations. This may critically alter model outcomes. We ask: how does the capacity for plasticity in populations with evolving genetic variance alter range margins that populations without the capacity for plasticity are expected to attain? We answered this question using computer simulations and analytical approximations. We found a critical plasticity cost above which the capacity for plasticity has no impact on the expected range of the population. Below the critical cost, by contrast, plasticity facilitates range expansion, extending the range in comparison to that expected for populations without plasticity. We further found that populations may evolve plasticity to buffer temporal environmental fluctuations, but only when the plasticity cost is below the critical cost. Thus, the cost of plasticity is a key factor involved in range expansions of populations with the potential to express plastic response in the adaptive trait. This article is part of the theme issue 'Species' ranges in the face of changing environments (part I)'.

The Effect of the Recombination Rate between Adaptive Loci on the Capacity of a Population to Expand Its Range.

AbstractPrevious theoretical work on range expansions over heterogeneous environments showed that there is a critical environmental gradient where range expansion stops. For populations with freely recombining loci underlying the trait under selection (hereafter, "adaptive loci"), the critical gradient in one-dimensional habitats depends on the fitness cost of dispersal and the strength of selection relative to genetic drift. Here, we extend the previous work in two directions and ask, What is the role of the recombination rate between the adaptive loci during range expansions? And what effect does the ability of selfing as opposed to obligate outcrossing have on range expansions? To answer these questions, we use computer simulations. We demonstrate that while reduced recombination rates between adaptive loci slow down range expansions as a result of poor purging of locally deleterious alleles at the expansion front, they may also allow a species to occupy a greater range. In addition, we find that the allowance of selfing may improve the ability of populations to expand their ranges, for example, because selfing among potentially rare high-fitness individuals facilitates the establishment and maintenance of locally well-adapted genotypes. We conclude that during range expansions there is a trade-off between positive and negative effects of recombination within and between individuals.

Inversions and genomic differentiation after secondary contact: When drift contributes to maintenance, not loss, of differentiation.

Due to their effects on reducing recombination, chromosomal inversions may play an important role in speciation by establishing and/or maintaining linked blocks of genes causing reproductive isolation (RI) between populations. This view fits empirical data indicating that inversions typically harbor loci involved in RI. However, previous computer simulations of infinite populations with two to four loci involved in RI implied that, even with gene flux as low as 10-8 per gamete, per generation between alternative arrangements, inversions may not have large, qualitative advantages over collinear regions in maintaining population differentiation after secondary contact. Here, we report that finite population sizes can help counteract the homogenizing consequences of gene flux, especially when several fitness-related loci reside within the inversion. In these cases, the persistence time of differentiation after secondary contact can be similar to when gene flux is absent and notably longer than the persistence time without inversions. Thus, despite gene flux, population differentiation may be maintained for up to 100,000 generations, during which time new incompatibilities and/or local adaptations might accumulate and facilitate progress toward speciation. How often these conditions are met in nature remains to be determined.

The impact of global selection on local adaptation and reproductive isolation.

Despite the homogenizing effect of strong gene flow between two populations, adaptation under symmetric divergent selection pressures results in partial reproductive isolation: adaptive substitutions act as local barriers to gene flow, and if divergent selection continues unimpeded, this will result in complete reproductive isolation of the two populations, i.e. speciation. However, a key issue in framing the process of speciation as a tension between local adaptation and the homogenizing force of gene flow is that the mutation process is blind to changes in the environment and therefore tends to limit adaptation. Here we investigate how globally beneficial mutations (GBMs) affect divergent local adaptation and reproductive isolation. When phenotypic divergence is finite, we show that the presence of GBMs limits local adaptation, generating a persistent genetic load at the loci that contribute to the trait under divergent selection and reducing genome-wide divergence. Furthermore, we show that while GBMs cannot prohibit the process of continuous differentiation, they induce a substantial delay in the genome-wide shutdown of gene flow. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

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.

Multiple chromosomal rearrangements in a hybrid zone between Littorina saxatilis ecotypes.

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 collected across a transect between contrasting habitats to detect chromosomal rearrangements de novo. We report 17 polymorphic rearrangements in a single locality for the coastal marine snail, Littorina saxatilis. Patterns of diversity in the field and of recombination in controlled crosses provide strong evidence that at least the majority of these rearrangements are inversions. Most show clinal changes in frequency between habitats, suggestive of divergent selection, but only one appears to be fixed for different arrangements in the two habitats. Consistent with widespread evidence for balancing selection on inversion polymorphisms, we argue that a combination of heterosis and divergent selection can explain the observed patterns and should be considered in other systems spanning environmental gradients.

Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow.

Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e., focuses on spatial patterns of allele frequency change) with system-specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome-wide SNP set from an ideally suited study organism, the intertidal snail Littorina saxatilis, which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non-neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Many non-neutral SNPs show relatively low levels of differentiation. We discuss potential reasons for this pattern, including loose linkage to selected variants, polygenic adaptation and a component of balancing selection within populations (which may be expected for inversions). Our work is in line with theory predicting a role for inversions in divergence, and emphasizes that genomic regions contributing to divergence may not always be accessible with methods purely based on allele frequency differences. These conclusions call for approaches that take spatial patterns of allele frequency change into account in other systems.

What genomic data can reveal about eco-evolutionary dynamics.

Recognition that evolution operates on the same timescale as ecological processes has motivated growing interest in eco-evolutionary dynamics. Nonetheless, generating sufficient data to test predictions about eco-evolutionary dynamics has proved challenging, particularly in natural contexts. Here we argue that genomic data can be integrated into the study of eco-evolutionary dynamics in ways that deepen our understanding of the interplay between ecology and evolution. Specifically, we outline five major questions in the study of eco-evolutionary dynamics for which genomic data may provide answers. Although genomic data alone will not be sufficient to resolve these challenges, integrating genomic data can provide a more mechanistic understanding of the causes of phenotypic change, help elucidate the mechanisms driving eco-evolutionary dynamics, and lead to more accurate evolutionary predictions of eco-evolutionary dynamics in nature.

Reciprocal transplants support a plasticity-first scenario during colonisation of a large hyposaline basin by a marine macro alga.

BACKGROUND: Establishing populations in ecologically marginal habitats may require substantial phenotypic changes that come about through phenotypic plasticity, local adaptation, or both. West-Eberhard's "plasticity-first" model suggests that plasticity allows for rapid colonisation of a new environment, followed by directional selection that develops local adaptation. Two predictions from this model are that (i) individuals of the original population have high enough plasticity to survive and reproduce in the marginal environment, and (ii) individuals of the marginal population show evidence of local adaptation. Individuals of the macroalga Fucus vesiculosus from the North Sea colonised the hyposaline (≥2-3‰) Baltic Sea less than 8000 years ago. The colonisation involved a switch from fully sexual to facultative asexual recruitment with release of adventitious branches that grow rhizoids and attach to the substratum. To test the predictions from the plasticity-first model we reciprocally transplanted F. vesiculosus from the original population (ambient salinity 24‰) and from the marginal population inside the Baltic Sea (ambient salinity 4‰). We also transplanted individuals of the Baltic endemic sister species F. radicans from 4 to 24‰. We assessed the degree of plasticity and local adaptation in growth and reproductive traits after 6 months by comparing the performance of individuals in 4 and 24‰. RESULTS: Branches of all individuals survived the 6 months period in both salinities, but grew better in their native salinity. Baltic Sea individuals more frequently developed asexual traits while North Sea individuals initiated formation of receptacles for sexual reproduction. CONCLUSIONS: Marine individuals of F. vesiculosus are highly plastic with respect to salinity and North Sea populations can survive the extreme hyposaline conditions of the Baltic Sea without selective mortality. Plasticity alone would thus allow for an initial establishment of this species inside the postglacial Baltic Sea at salinities where reproduction remains functional. Since establishment, the Baltic Sea populations have evolved adaptations to extreme hyposaline waters and have in addition evolved asexual recruitment that, however, tends to impede local adaptation. Overall, our results support the "plasticity-first" model for the initial colonisation of the Baltic Sea by Fucus vesiculosus.