TY - GEN AB - Domestication is a human-induced selection process that imprints the genomes of domesticated populations over a short evolutionary time scale, and that occurs in a given demographic context. Reconstructing historical gene flow, effective population size changes and their timing is therefore of fundamental interest to understand how plant demography and human selection jointly shape genomic divergence during domestication. Yet, the comparison under a single statistical framework of independent domestication histories across different crop species has been little evaluated so far. Thus, it is unclear whether domestication leads to convergent demographic changes that similarly affect crop genomes. To address this question, we used existing and new transcriptome data on three crop species of Solanaceae (eggplant, pepper and tomato), together with their close wild relatives. We fitted twelve demographic models of increasing complexity on the unfolded joint allele frequency spectrum for each wild/crop pair, and we found evidence for both shared and species-specific demographic processes between species. A convergent history of domestication with gene-flow was inferred for all three species, along with evidence of strong reduction in the effective population size during the cultivation stage of tomato and pepper. The absence of any reduction in size of the crop in eggplant stands out from the classical view of the domestication process; as does the existence of a “protracted period” of management before cultivation. Our results also suggest divergent management strategies of modern cultivars among species as their current demography substantially differs. Finally, the timing of domestication is species-specific and supported by the few historical records available. AU - Arnoux, Stephanie AU - Fraisse, Christelle AU - Sauvage, Christopher ID - 13065 TI - VCF files of synonymous SNPs related to: Genomic inference of complex domestication histories in three Solanaceae species ER - TY - JOUR AB - 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. AU - Perini, Samuel AU - Rafajlović, Marina AU - Westram, Anja M AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 7995 IS - 7 JF - Evolution SN - 00143820 TI - Assortative mating, sexual selection, and their consequences for gene flow in Littorina VL - 74 ER - TY - GEN AB - 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. AU - Perini, Samuel AU - Rafajlovic, Marina AU - Westram, Anja M AU - Johannesson, Kerstin AU - Butlin, Roger ID - 8809 TI - Data from: Assortative mating, sexual selection and their consequences for gene flow in Littorina ER - TY - JOUR AU - Barton, Nicholas H ID - 8112 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological Sciences SN - 0962-8436 TI - On the completion of speciation VL - 375 ER - TY - JOUR AB - 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 from partial to strong reproductive isolation (RI) and the completion of speciation. We argue that the evolution of strong RI is likely to involve different processes, or new interactions among processes, compared with the evolution of the first reproductive barriers. Transition to strong RI may be brought about by changing external conditions, for example, following secondary contact. However, the increasing levels of RI themselves create opportunities for new barriers to evolve and, and interaction or coupling among barriers. These changing processes may depend on genomic architecture and leave detectable signals in the genome. We outline outstanding questions and suggest more theoretical and empirical work, considering both patterns and processes associated with strong RI, is needed to understand how speciation is completed. AU - Kulmuni, Jonna AU - Butlin, Roger K. AU - Lucek, Kay AU - Savolainen, Vincent AU - Westram, Anja M ID - 8168 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological sciences SN - 0962-8436 TI - Towards the completion of speciation: The evolution of reproductive isolation beyond the first barriers VL - 375 ER - TY - JOUR AB - 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 genotyping, we inferred (i) the evolutionary relationships, (ii) the strength of RI, and (iii) the demographic history of divergence between two broadly sympatric taxa of intertidal snail. Despite being cryptic, based on external morphology, Littorina arcana and Littorina saxatilis differ in their mode of female reproduction (egg-laying versus brooding), which may generate a strong post-zygotic barrier. We show that egg-laying and brooding snails are closely related, but genetically distinct. Genotyping of 3092 snails from three locations failed to recover any recent hybrid or backcrossed individuals, confirming that RI is strong. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The presence of strong, asymmetrical RI was further supported by demographic analysis of these populations. Although the taxa are currently broadly sympatric, demographic modelling suggests that they initially diverged during a short period of geographical separation involving very low gene flow. Our study suggests that some geographical separation may kick-start the evolution of strong RI, facilitating subsequent coexistence of taxa in sympatry. The strength of RI needed to achieve sympatry and the subsequent effect of sympatry on RI remain open questions. AU - Stankowski, Sean AU - Westram, Anja M AU - Zagrodzka, Zuzanna B. AU - Eyres, Isobel AU - Broquet, Thomas AU - Johannesson, Kerstin AU - Butlin, Roger K. ID - 8167 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological Sciences TI - The evolution of strong reproductive isolation between sympatric intertidal snails VL - 375 ER - TY - JOUR AB - Many recent studies have addressed the mechanisms operating during the early stages of speciation, but surprisingly few studies have tested theoretical predictions on the evolution of strong reproductive isolation (RI). To help address this gap, we first undertook a quantitative review of the hybrid zone literature for flowering plants in relation to reproductive barriers. Then, using Populus as an exemplary model group, we analysed genome-wide variation for phylogenetic tree topologies in both early- and late-stage speciation taxa to determine how these patterns may be related to the genomic architecture of RI. Our plant literature survey revealed variation in barrier complexity and an association between barrier number and introgressive gene flow. Focusing on Populus, our genome-wide analysis of tree topologies in speciating poplar taxa points to unusually complex genomic architectures of RI, consistent with earlier genome-wide association studies. These architectures appear to facilitate the ‘escape’ of introgressed genome segments from polygenic barriers even with strong RI, thus affecting their relationships with recombination rates. Placed within the context of the broader literature, our data illustrate how phylogenomic approaches hold great promise for addressing the evolution and temporary breakdown of RI during late stages of speciation. AU - Shang, Huiying AU - Hess, Jaqueline AU - Pickup, Melinda AU - Field, David AU - Ingvarsson, Pär K. AU - Liu, Jianquan AU - Lexer, Christian ID - 8169 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological Sciences TI - Evolution of strong reproductive isolation in plants: Broad-scale patterns and lessons from a perennial model group VL - 375 ER - TY - GEN AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA. Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 9799 TI - Simulation code for Fig S1 from the distribution of epistasis on simple fitness landscapes ER - TY - GEN AB - Fitness interactions between mutations can influence a population’s evolution in many different ways. While epistatic effects are difficult to measure precisely, important information is captured by the mean and variance of log fitnesses for individuals carrying different numbers of mutations. We derive predictions for these quantities from a class of simple fitness landscapes, based on models of optimizing selection on quantitative traits. We also explore extensions to the models, including modular pleiotropy, variable effect sizes, mutational bias and maladaptation of the wild type. We illustrate our approach by reanalysing a large dataset of mutant effects in a yeast snoRNA. Though characterized by some large epistatic effects, these data give a good overall fit to the non-epistatic null model, suggesting that epistasis might have limited influence on the evolutionary dynamics in this system. We also show how the amount of epistasis depends on both the underlying fitness landscape and the distribution of mutations, and so is expected to vary in consistent ways between new mutations, standing variation and fixed mutations. AU - Fraisse, Christelle AU - Welch, John J. ID - 9798 TI - Simulation code for Fig S2 from the distribution of epistasis on simple fitness landscapes ER - TY - JOUR AB - The biotic interactions hypothesis posits that biotic interactions are more important drivers of adaptation closer to the equator, evidenced by “stronger” contemporary interactions (e.g. greater interaction rates) and/or patterns of trait evolution consistent with a history of stronger interactions. Support for the hypothesis is mixed, but few studies span tropical and temperate regions while experimentally controlling for evolutionary history. Here, we integrate field observations and common garden experiments to quantify the relative importance of pollination and herbivory in a pair of tropical‐temperate congeneric perennial herbs. Phytolacca rivinoides and P. americana are pioneer species native to the Neotropics and the eastern USA, respectively. We compared plant‐pollinator and plant‐herbivore interactions between three tropical populations of P. rivinoides from Costa Rica and three temperate populations of P. americana from its northern range edge in Michigan and Ohio. For some metrics of interaction importance, we also included three subtropical populations of P. americana from its southern range edge in Florida. This approach confounds species and region but allows us, uniquely, to measure complementary proxies of interaction importance across a tropical‐temperate range in one system. To test the prediction that lower‐latitude plants are more reliant on insect pollinators, we quantified floral display and reward, insect visitation rates, and self‐pollination ability (autogamy). To test the prediction that lower‐latitude plants experience more herbivore pressure, we quantified herbivory rates, herbivore abundance, and leaf palatability. We found evidence supporting the biotic interactions hypothesis for most comparisons between P. rivinoides and north‐temperate P. americana (floral display, insect visitation, autogamy, herbivory, herbivore abundance, and young‐leaf palatability). Results for subtropical P. americana populations, however, were typically not intermediate between P. rivinoides and north‐temperate P. americana, as would be predicted by a linear latitudinal gradient in interaction importance. Subtropical young‐leaf palatability was intermediate, but subtropical mature leaves were the least palatable, and pollination‐related traits did not differ between temperate and subtropical regions. These nonlinear patterns of interaction importance suggest future work to relate interaction importance to climatic or biotic thresholds. In sum, we found that the biotic interactions hypothesis was more consistently supported at the larger spatial scale of our study. AU - Baskett, Carina AU - Schroeder, Lucy AU - Weber, Marjorie G. AU - Schemske, Douglas W. ID - 7236 IS - 1 JF - Ecological Monographs SN - 0012-9615 TI - Multiple metrics of latitudinal patterns in insect pollination and herbivory for a tropical‐temperate congener pair VL - 90 ER - TY - JOUR AB - 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 role of post‐zygotic barriers due to selection against hybrids remains unclear. High embryo abortion rates in this species could indicate the presence of such barriers. Post‐zygotic barriers might include genetic incompatibilities (e.g. Dobzhansky–Muller incompatibilities) but also maladaptation, both expected to be most pronounced in contact zones. In addition, embryo abortion might reflect physiological stress on females and embryos independent of any genetic stress. We examined all embryos of >500 females sampled outside and inside contact zones of three populations in Sweden. Females' clutch size ranged from 0 to 1,011 embryos (mean 130 ± 123), and abortion rates varied between 0% and 100% (mean 12%). We described female genotypes by using a hybrid index based on hundreds of SNPs differentiated between ecotypes with which we characterized female genotypes. We also calculated female SNP heterozygosity and inversion karyotype. Clutch size did not vary with female hybrid index, and abortion rates were only weakly related to hybrid index in two sites but not at all in a third site. No additional variation in abortion rate was explained by female SNP heterozygosity, but increased female inversion heterozygosity added slightly to increased abortion. Our results show only weak and probably biologically insignificant post‐zygotic barriers contributing to ecotype divergence, and the high and variable abortion rates were marginally, if at all, explained by hybrid index of females. AU - Johannesson, Kerstin AU - Zagrodzka, Zuzanna AU - Faria, Rui AU - Westram, Anja M AU - Butlin, Roger K. ID - 7205 IS - 3 JF - Journal of Evolutionary Biology SN - 1010061X TI - Is embryo abortion a post-zygotic barrier to gene flow between Littorina ecotypes? VL - 33 ER - TY - THES AB - This thesis concerns itself with the interactions of evolutionary and ecological forces and the consequences on genetic diversity and the ultimate survival of populations. It is important to understand what signals processes leave on the genome and what we can infer from such data, which is usually abundant but noisy. Furthermore, understanding how and when populations adapt or go extinct is important for practical purposes, such as the genetic management of populations, as well as for theoretical questions, since local adaptation can be the first step toward speciation. In Chapter 2, we introduce the method of maximum entropy to approximate the demographic changes of a population in a simple setting, namely the logistic growth model with immigration. We show that this method is not only a powerful tool in physics but can be gainfully applied in an ecological framework. We investigate how well it approximates the real behavior of the system, and find that is does so, even in unexpected situations. Finally, we illustrate how it can model changing environments. In Chapter 3, we analyze the co-evolution of allele frequencies and population sizes in an infinite island model. We give conditions under which polygenic adaptation to a rare habitat is possible. The model we use is based on the diffusion approximation, considers eco-evolutionary feedback mechanisms (hard selection), and treats both drift and environmental fluctuations explicitly. We also look at limiting scenarios, for which we derive analytical expressions. In Chapter 4, we present a coalescent based simulation tool to obtain patterns of diversity in a spatially explicit subdivided population, in which the demographic history of each subpopulation can be specified. We compare the results to existing predictions, and explore the relative importance of time and space under a variety of spatial arrangements and demographic histories, such as expansion and extinction. In the last chapter, we give a brief outlook to further research. AU - Szep, Eniko ID - 8574 TI - Local adaptation in metapopulations ER - TY - DATA AB - Here are the research data underlying the publication "Estimating inbreeding and its effects in a long-term study of snapdragons (Antirrhinum majus)". Further information are summed up in the README document. The files for this record have been updated and are now found in the linked DOI https://doi.org/10.15479/AT:ISTA:9192. AU - Arathoon, Louise S ID - 8254 TI - Estimating inbreeding and its effects in a long-term study of snapdragons (Antirrhinum majus) ER - TY - GEN AB - More than 100 years after Grigg’s influential analysis of species’ borders, the causes of limits to species’ ranges still represent a puzzle that has never been understood with clarity. The topic has become especially important recently as many scientists have become interested in the potential for species’ ranges to shift in response to climate change—and yet nearly all of those studies fail to recognise or incorporate evolutionary genetics in a way that relates to theoretical developments. I show that range margins can be understood based on just two measurable parameters: (i) the fitness cost of dispersal—a measure of environmental heterogeneity—and (ii) the strength of genetic drift, which reduces genetic diversity. Together, these two parameters define an ‘expansion threshold’: adaptation fails when genetic drift reduces genetic diversity below that required for adaptation to a heterogeneous environment. When the key parameters drop below this expansion threshold locally, a sharp range margin forms. When they drop below this threshold throughout the species’ range, adaptation collapses everywhere, resulting in either extinction or formation of a fragmented metapopulation. Because the effects of dispersal differ fundamentally with dimension, the second parameter—the strength of genetic drift—is qualitatively different compared to a linear habitat. In two-dimensional habitats, genetic drift becomes effectively independent of selection. It decreases with ‘neighbourhood size’—the number of individuals accessible by dispersal within one generation. Moreover, in contrast to earlier predictions, which neglected evolution of genetic variance and/or stochasticity in two dimensions, dispersal into small marginal populations aids adaptation. This is because the reduction of both genetic and demographic stochasticity has a stronger effect than the cost of dispersal through increased maladaptation. The expansion threshold thus provides a novel, theoretically justified, and testable prediction for formation of the range margin and collapse of the species’ range. AU - Polechova, Jitka ID - 9839 TI - Data from: Is the sky the limit? On the expansion threshold of a species' range ER - TY - JOUR AB - 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, and gene flux between arrangements. Inversion polymorphisms are maintained by different processes, for example, divergent or balancing selection, or a mix of multiple processes. Moreover, the relative roles of selection, drift, mutation, and recombination will change over the lifetime of an inversion and within its area of distribution. We believe inversions are central to the evolution of many species, but we need many more data and new models to understand the complex mechanisms involved. AU - Faria, Rui AU - Johannesson, Kerstin AU - Butlin, Roger K. AU - Westram, Anja M ID - 5911 IS - 3 JF - Trends in Ecology and Evolution SN - 01695347 TI - Evolving inversions VL - 34 ER - TY - JOUR AB - Pollinators display a remarkable diversity of foraging strategies with flowering plants, from primarily mutualistic interactions to cheating through nectar robbery. Despite numerous studies on the effect of nectar robbing on components of plant fitness, its contribution to reproductive isolation is unclear. We experimentally tested the impact of different pollinator strategies in a natural hybrid zone between two subspecies of Antirrhinum majus with alternate flower colour guides. On either side of a steep cline in flower colour between Antirrhinum majus pseudomajus (magenta) and A. m. striatum (yellow), we quantified the behaviour of all floral visitors at different time points during the flowering season. Using long-run camera surveys, we quantify the impact of nectar robbing on the number of flowers visited per inflorescence and the flower probing time. We further experimentally tested the effect of nectar robbing on female reproductive success by manipulating the intensity of robbing. While robbing increased over time the number of legitimate visitors tended to decrease concomitantly. We found that the number of flowers pollinated on a focal inflorescence decreased with the number of prior robbing events. However, in the manipulative experiment, fruit set and fruit volume did not vary significantly between low robbing and control treatments. Our findings challenge the idea that robbers have a negative impact on plant fitness through female function. This study also adds to our understanding of the components of pollinator-mediated reproductive isolation and the maintenance of Antirrhinum hybrid zones. AU - Andalo, Christophe AU - Burrus, Monique AU - Paute, Sandrine AU - Lauzeral, Christine AU - Field, David ID - 5680 IS - 1 JF - Botany Letters SN - 23818107 TI - Prevalence of legitimate pollinators and nectar robbers and the consequences for fruit set in an Antirrhinum majus hybrid zone VL - 166 ER - TY - JOUR AB - The evolution of new species is made easier when traits under divergent ecological selection are also mating cues. Such ecological mating cues are now considered more common than previously thought, but we still know little about the genetic changes underlying their evolution or more generally about the genetic basis for assortative mating behaviors. Both tight physical linkage and the existence of large-effect preference loci will strengthen genetic associations between behavioral and ecological barriers, promoting the evolution of assortative mating. The warning patterns of Heliconius melpomene and H. cydno are under disruptive selection due to increased predation of nonmimetic hybrids and are used during mate recognition. We carried out a genome-wide quantitative trait locus (QTL) analysis of preference behaviors between these species and showed that divergent male preference has a simple genetic basis. We identify three QTLs that together explain a large proportion (approximately 60%) of the difference in preference behavior observed between the parental species. One of these QTLs is just 1.2 (0-4.8) centiMorgans (cM) from the major color pattern gene optix, and, individually, all three have a large effect on the preference phenotype. Genomic divergence between H. cydno and H. melpomene is high but broadly heterogenous, and admixture is reduced at the preference-optix color pattern locus but not the other preference QTLs. The simple genetic architecture we reveal will facilitate the evolution and maintenance of new species despite ongoing gene flow by coupling behavioral and ecological aspects of reproductive isolation. AU - Merrill, Richard M. AU - Rastas, Pasi AU - Martin, Simon H. AU - Melo Hurtado, Maria C AU - Barker, Sarah AU - Davey, John AU - Mcmillan, W. Owen AU - Jiggins, Chris D. ID - 6022 IS - 2 JF - PLoS Biology TI - Genetic dissection of assortative mating behavior VL - 17 ER - TY - GEN AU - Merrill, Richard M. AU - Rastas, Pasi AU - Martin, Simon H. AU - Melo Hurtado, Maria C AU - Barker, Sarah AU - Davey, John AU - Mcmillan, W. Owen AU - Jiggins, Chris D. ID - 9801 TI - Raw behavioral data ER - TY - JOUR AB - 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. AU - Faria, Rui AU - Chaube, Pragya AU - Morales, Hernán E. AU - Larsson, Tomas AU - Lemmon, Alan R. AU - Lemmon, Emily M. AU - Rafajlović, Marina AU - Panova, Marina AU - Ravinet, Mark AU - Johannesson, Kerstin AU - Westram, Anja M AU - Butlin, Roger K. ID - 6095 IS - 6 JF - Molecular Ecology SN - 0962-1083 TI - Multiple chromosomal rearrangements in a hybrid zone between Littorina saxatilis ecotypes VL - 28 ER - TY - JOUR AB - Great care is needed when interpreting claims about the genetic basis of human variation based on data from genome-wide association studies. AU - Barton, Nicholas H AU - Hermisson, Joachim AU - Nordborg, Magnus ID - 6230 JF - eLife TI - Why structure matters VL - 8 ER -