TY - JOUR AB - Empirical essays of fitness landscapes suggest that they may be rugged, that is having multiple fitness peaks. Such fitness landscapes, those that have multiple peaks, necessarily have special local structures, called reciprocal sign epistasis (Poelwijk et al. in J Theor Biol 272:141–144, 2011). Here, we investigate the quantitative relationship between the number of fitness peaks and the number of reciprocal sign epistatic interactions. Previously, it has been shown (Poelwijk et al. in J Theor Biol 272:141–144, 2011) that pairwise reciprocal sign epistasis is a necessary but not sufficient condition for the existence of multiple peaks. Applying discrete Morse theory, which to our knowledge has never been used in this context, we extend this result by giving the minimal number of reciprocal sign epistatic interactions required to create a given number of peaks. AU - Saona Urmeneta, Raimundo J AU - Kondrashov, Fyodor AU - Khudiakova, Kseniia ID - 11447 IS - 8 JF - Bulletin of Mathematical Biology KW - Computational Theory and Mathematics KW - General Agricultural and Biological Sciences KW - Pharmacology KW - General Environmental Science KW - General Biochemistry KW - Genetics and Molecular Biology KW - General Mathematics KW - Immunology KW - General Neuroscience SN - 0092-8240 TI - Relation between the number of peaks and the number of reciprocal sign epistatic interactions VL - 84 ER - TY - JOUR AB - 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 break-up of favourable combinations of alleles across multiple loci, genetic architectures that reduce recombination, like chromosomal inversions, can make an important contribution to local adaptation. However, little is known about whether inversions also contribute disproportionately to parallel evolution. Our aim here is to highlight this knowledge gap, to showcase existing studies, and to illustrate the differences between genomic architectures with and without inversions using simple models. We predict that by generating stronger effective selection, inversions can sometimes speed up the parallel adaptive process or enable parallel adaptation where it would be impossible otherwise, but this is highly dependent on the spatial setting. We highlight that further empirical work is needed, in particular to cover a broader taxonomic range and to understand the relative importance of inversions compared to genomic regions without inversions. AU - Westram, Anja M AU - Faria, Rui AU - Johannesson, Kerstin AU - Butlin, Roger AU - Barton, Nicholas H ID - 11546 IS - 1856 JF - Philosophical Transactions of the Royal Society B: Biological Sciences KW - General Agricultural and Biological Sciences KW - General Biochemistry KW - Genetics and Molecular Biology SN - 0962-8436 TI - Inversions and parallel evolution VL - 377 ER - TY - JOUR AB - Spatially explicit population genetic models have long been developed, yet have rarely been used to test hypotheses about the spatial distribution of genetic diversity or the genetic divergence between populations. Here, we use spatially explicit coalescence simulations to explore the properties of the island and the two-dimensional stepping stone models under a wide range of scenarios with spatio-temporal variation in deme size. We avoid the simulation of genetic data, using the fact that under the studied models, summary statistics of genetic diversity and divergence can be approximated from coalescence times. We perform the simulations using gridCoal, a flexible spatial wrapper for the software msprime (Kelleher et al., 2016, Theoretical Population Biology, 95, 13) developed herein. In gridCoal, deme sizes can change arbitrarily across space and time, as well as migration rates between individual demes. We identify different factors that can cause a deviation from theoretical expectations, such as the simulation time in comparison to the effective deme size and the spatio-temporal autocorrelation across the grid. Our results highlight that FST, a measure of the strength of population structure, principally depends on recent demography, which makes it robust to temporal variation in deme size. In contrast, the amount of genetic diversity is dependent on the distant past when Ne is large, therefore longer run times are needed to estimate Ne than FST. Finally, we illustrate the use of gridCoal on a real-world example, the range expansion of silver fir (Abies alba Mill.) since the last glacial maximum, using different degrees of spatio-temporal variation in deme size. AU - Szep, Eniko AU - Trubenova, Barbora AU - Csilléry, Katalin ID - 11640 IS - 8 JF - Molecular Ecology Resources SN - 1755-098X TI - Using gridCoal to assess whether standard population genetic theory holds in the presence of spatio-temporal heterogeneity in population size VL - 22 ER - TY - JOUR AB - 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 recombination suppression but their precise role in sex chromosome evolution remains unclear. Because local adaptation is frequently facilitated through the suppression of recombination between adaptive loci by chromosomal inversions, there is potential for inversions that cover sex-determining regions to be involved in local adaptation as well, particularly if habitat variation creates environment-dependent sexual antagonism. With these processes in mind, we investigated sex determination in a well-studied example of local adaptation within a species: the intertidal snail, Littorina saxatilis. Using SNP data from a Swedish hybrid zone, we find novel evidence for a female-heterogametic sex determination system that is restricted to one ecotype. Our results suggest that four putative chromosomal inversions, two previously described and two newly discovered, span the putative sex chromosome pair. We determine their differing associations with sex, which suggest distinct strata of differing ages. The same inversions are found in the second ecotype but do not show any sex association. The striking disparity in inversion-sex associations between ecotypes that are connected by gene flow across a habitat transition that is just a few meters wide indicates a difference in selective regime that has produced a distinct barrier to the spread of the newly discovered sex-determining region between ecotypes. Such sex chromosome-environment interactions have not previously been uncovered in L. saxatilis and are known in few other organisms. A combination of both sex-specific selection and divergent natural selection is required to explain these highly unusual patterns. AU - Hearn, Katherine E. AU - Koch, Eva L. AU - Stankowski, Sean AU - Butlin, Roger K. AU - Faria, Rui AU - Johannesson, Kerstin AU - Westram, Anja M ID - 12001 IS - 5 JF - Evolution Letters TI - Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis VL - 6 ER - TY - JOUR AB - Polygenic adaptation is thought to be ubiquitous, yet remains poorly understood. Here, we model this process analytically, in the plausible setting of a highly polygenic, quantitative trait that experiences a sudden shift in the fitness optimum. We show how the mean phenotype changes over time, depending on the effect sizes of loci that contribute to variance in the trait, and characterize the allele dynamics at these loci. Notably, we describe the two phases of the allele dynamics: The first is a rapid phase, in which directional selection introduces small frequency differences between alleles whose effects are aligned with or opposed to the shift, ultimately leading to small differences in their probability of fixation during a second, longer phase, governed by stabilizing selection. As we discuss, key results should hold in more general settings and have important implications for efforts to identify the genetic basis of adaptation in humans and other species. AU - Hayward, Laura AU - Sella, Guy ID - 12157 JF - eLife KW - General Immunology and Microbiology KW - General Biochemistry KW - Genetics and Molecular Biology KW - General Medicine KW - General Neuroscience TI - Polygenic adaptation after a sudden change in environment VL - 11 ER - TY - JOUR AB - Kerstin Johannesson is a marine ecologist and evolutionary biologist based at the Tjärnö Marine Laboratory of the University of Gothenburg, which is situated in the beautiful Kosterhavet National Park on the Swedish west coast. Her work, using marine periwinkles (especially Littorina saxatilis and L. fabalis) as main model systems, has made a remarkable contribution to marine evolutionary biology and our understanding of local adaptation and its genetic underpinnings. AU - Westram, Anja M AU - Butlin, Roger ID - 12166 IS - 1 JF - Molecular Ecology KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0962-1083 TI - Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize VL - 32 ER - TY - JOUR AB - Hybrid speciation—the origin of new species resulting from the hybridization of genetically divergent lineages—was once considered rare, but genomic data suggest that it may occur more often than once thought. In this study, Noguerales and Ortego found genomic evidence supporting the hybrid origin of a grasshopper that is able to exploit a broader range of host plants than either of its putative parents. AU - Stankowski, Sean ID - 12234 IS - 11 JF - Evolution KW - General Agricultural and Biological Sciences KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0014-3820 TI - Digest: On the origin of a possible hybrid species VL - 76 ER - TY - JOUR AB - Chromosomal inversions have been shown to play a major role in a 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 estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence. AU - Koch, Eva L. AU - Ravinet, Mark AU - Westram, Anja M AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 12247 IS - 10 JF - Evolution KW - General Agricultural and Biological Sciences KW - Genetics KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 0014-3820 TI - Genetic architecture of repeated phenotypic divergence in Littorina saxatilis evolution VL - 76 ER - TY - GEN AB - 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 estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence. AU - Koch, Eva AU - Ravinet, Mark AU - Westram, Anja M AU - Jonannesson, Kerstin AU - Butlin, Roger ID - 13066 TI - Data from: Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution ER - TY - JOUR AB - Reproductive isolation (RI) is a core concept in evolutionary biology. It has been the central focus of speciation research since the modern synthesis and is the basis by which biological species are defined. Despite this, the term is used in seemingly different ways, and attempts to quantify RI have used very different approaches. After showing that the field lacks a clear definition of the term, we attempt to clarify key issues, including what RI is, how it can be quantified in principle, and how it can be measured in practice. Following other definitions with a genetic focus, we propose that RI is a quantitative measure of the effect that genetic differences between populations have on gene flow. Specifically, RI compares the flow of neutral alleles in the presence of these genetic differences to the flow without any such differences. RI is thus greater than zero when genetic differences between populations reduce the flow of neutral alleles between populations. We show how RI can be quantified in a range of scenarios. A key conclusion is that RI depends strongly on circumstances—including the spatial, temporal and genomic context—making it difficult to compare across systems. After reviewing methods for estimating RI from data, we conclude that it is difficult to measure in practice. We discuss our findings in light of the goals of speciation research and encourage the use of methods for estimating RI that integrate organismal and genetic approaches. AU - Westram, Anja M AU - Stankowski, Sean AU - Surendranadh, Parvathy AU - Barton, Nicholas H ID - 12264 IS - 9 JF - Journal of Evolutionary Biology KW - Ecology KW - Evolution KW - Behavior and Systematics SN - 1010-061X TI - What is reproductive isolation? VL - 35 ER -