Together with our finding that mating pattern was very similar among islands and between ecotypes, this suggests that the pattern is ancestral and strongly conserved. 1 to pop. The only reliable phenotypic character distinguishing the species is their reproductive mode: while both species show direct development (i.e. The mating pattern across all islands, fitted by the nonhierarchical model, followed a right‐skewed distribution. PC2 (8.2%) and PC3 (6.7%) were associated with differences that were specific to English L. saxatilis and English L. arcana, respectively. Table S5. Mar., Vol. Comparison between the hierarchical model with the subset of variables and the full hierarchical model. By “mating pattern,” we mean the function that predicts the probability of mating, given an encounter between a male and female with specified phenotypes. S5), or for all individuals (third column in Fig. 2018). M12, migration from pop. However, there is a danger that the classification takes on a life of its own: although it may have been clear, originally, that a continuum was being subdivided for convenience, there is a danger that the allocation of case studies to categories becomes an end in itself. Despite their close evolutionary relationships and possible evidence for gene flow, it is clear that this sequenced sample does not include any individuals that are the product of recent hybridization between L. arcana and L. saxatilis. Each mating trial (transect‐reference pair) was unique (i.e., involved a pair of snails that was not brought together again) and it was monitored for 2 hours during which male mounting activity was recorded. 2). The best model, with the lowest Akaike information criterion (), included effects of size ratio squared and various interaction terms, including two‐way interactions between and island, and between size ratio and both shape and island, although their effects were relatively small. To simulate reproduction within each mode without gene flow, we generated individuals for each mode using the observed sample sizes in each location (six groups) by drawing an allele frequency for each locus from a binomial distribution with the observed allele frequency and sample size (of alleles) and then used this frequency to draw genotypes for each locus, by binomial sampling with sample size 2. The first principal component (PC1), which explained 9.8% of the variation in the data, clearly separated egg-laying and brooding individuals. In L. saxatilis, the genomic landscape of ecotype divergence is characterized by a small number of highly differentiated regions, most of which overlap with putative chromosomal inversions that appear to be involved in local adaption in multiple locations [18–20]. Selection resulting from the reduced fitness of hybrids can, in theory, increase reproductive isolation (reinforcement) but the conditions required are quite stringent (Liou and Price 1994; Price 2008; but see Servedio and Noor 2003). The SNP genotype dataset, SNP design information and scripts used to analyse the data are available at 3 and S4). The Wave and the Crab ecotypes (simply “Wave” and “Crab” in the following) are encountered widely in wave‐exposed and crab‐rich habitats, respectively, over the species’ North Eastern Atlantic distribution (Johannesson et al. Mill. Brooding is a derived condition that appears to have evolved recently (1.7–0.06 Ma [29]) from an ancestral egg-laying population. These models allow us to test the effect of assortative mating alone (SimM0), assortative mating combined with a shift in the optimum trait ratio corresponding to either the observed mean (SimMR) or the observed optimum (SimOR) but without asymmetry, or the full observed mating model including skew (AS). 4E). S.S. wrote the manuscript with input from the other authors. The most likely explanation for this is strong selection for large size imposed on both sexes by crab predation in the Crab environment (Johannesson 1986). First, we quantified the mating probability given encounters between snails with a wide range of sizes and shapes. Admixture used the same statistical model as the program Structure [56], but calculates ancestry much more rapidly and accurately by using a numerical optimization algorithm [55]. 65 No. Further evolution of the mating pattern may be more likely in Spanish populations where there is more widespread contact (Galindo et al. Whatever the nature of assortative mating and sexual selection, it is important to quantify their contribution to the overall barrier to gene flow during the process of speciation. Assortative mating and sexual selection in the CZA, CZC and CZD transects. Using whole-genome sequences and SNP genotyping of large field-collected samples, our study has clarified the evolutionary and reproductive relationships between L. arcana and L. saxatilis using samples spanning a large part of their range [24]. 2011; Smadja and Butlin 2011; Kopp et al. The most obvious candidate for a barrier trait is the difference in female reproductive strategy between the taxa, which includes a difference in both the mode (egg-laying in L. arcana versus brooding in L. saxatilis) and timing (seasonal in L. arcana versus year-round in L. saxatilis) of reproduction. As the directional component of sexual selection moves the male mean size further from the environmental optimum, the strength of natural selection back toward the optimum increases. 2). The same procedure was used to estimate an ‘L. In the light of the current distributions of these taxa, we propose the following biogeographic history as a working hypothesis for their divergence: the brooding strategy—the trait that defines L. saxatilis—probably arose in a location where the egg-laying reproductive strategy is now absent. - Volume 79 Issue 5 - Susan L. Hull, John Grahame, Peter J. In addition, we fitted the spatial pattern of the hybrid index obtained in our simulations to a constant value, independent of the spatial position (which is an expected pattern under neutral evolution), to check whether a clinal pattern explains our hybrid‐index data better than a neutral‐evolution model (using AIC). FIG. This adds to the evidence that L. neglecta is not a distinct species, but an ecotype of L. saxatilis. Our data show consistently greater size dimorphism in the Wave ecotype than in the Crab ecotype (Figs. For each mating pair, we had information about whether a mating event was observed or not, the island where the transect snail was collected (CZA, CZB, CZC, or CZD), transect snail shape, the ecotype of the reference snail (Crab and Wave), the sex of the transect snail (and therefore of the reference snail), and the sizes of the two snails, which were used to calculate the ratio between the female and male size for each mating pair. and you may need to create a new Wiley Online Library account. The full text of this article hosted at is unavailable due to technical difficulties. 2011). Assortative mating might depend on a matching rule where there is no separation of signal and preference and so they necessarily coevolve. For males, this was only true under the random mating model and under the SimM0 model (Gaussian mating probability with optimum at zero, i.e., with the maximum mating probability for equal‐sized males and females; see Figs. Here, σs is the inverse of the strength of natural selection. For both simulations, hybrid index scores were calculated as described for the real data. Mating trials were performed indoors under constant light and at room temperature. If the features of the observed distributions (i.e. 2005). Figure S6. 2018; Faria et al. However, the differences between the three symmetric mating models were subtle. S.S., A.M.W., R.K.B. If you do not receive an email within 10 minutes, your email address may not be registered, RI appears to be even stronger in Spain (FST range = 0.09–0.12 [20]), as the ecotypes are able to coexist in a narrow zone with much lower admixture than in Sweden [23]. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The use of transect snails from throughout the transects provided a wide range of trait values (and trait value combinations between males and females). Any queries (other than missing content) should be directed to the corresponding author for the article. Here, we investigated the contribution to reproductive isolation of shell size, a single trait with effects on both ecological and sexual isolation between Crab and Wave ecotypes of Littorina saxatilis. Comparing evolvability and variability of quantitative traits, Assortative mating between two distinct micro allopatric populations of, Assortative mating in hybrid zones is remarkably ineffective in promoting speciation, Assortative mating in animals and its role for speciation, Selection and migration in two distinct phenotypes of, Incipient reproductive isolation between two sympatric morphs of the intertidal snail, Male discrimination of female mucous trails permits assortative mating in a marine snail species, Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation, Non‐random paternity of offspring in a highly promiscuous marine snail suggests postcopulatory sexual selection, Speciation by natural and sexual selection: models and experiments, Mechanisms of assortative mating in speciation with gene flow: connecting theory and empirical research, Models of speciation by sexual selection on polygenic traits, Adaptation to dislodgement risk on wave‐swept rocky shores in the snail, Speciation by reinforcement of premating isolation, The strength and genetic basis of reproductive isolating barriers in flowering plants, Hybridization as an invasion of the genome, Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles, Speciation in nature: the threespine stickleback model systems, Divergent warning patterns contribute to assortative mating between incipient, Genetic dissection of assortative mating behavior, Genomic architecture of parallel ecological divergence: beyond a single environmental contrast. The contributions of individual barriers can be estimated by breaking down reproductive isolation into its components (Coyne and Orr 2004, pp. Finally, parameters and are scaling parameters proportional to the overall minimum and maximum proportion of trials in which mating occurred: we call them the “mating baseline” and the “mating rate”, respectively (Fig. (2018). 2018), with obvious benefits in terms of simplicity and tractability. Raw reads were mapped to the L. saxatilis version 1 reference genome [18] using the BWAmem algorithm [49]. Females were assigned to L. saxatilis if a brood pouch containing embryos was present. E, England; F, France; W, Wales. 2019). We then calculated the unfolded JSFS between L. arcana and L. saxatilis, separately for each location, using L. compressa as an outgroup to polarize alleles as ancestral or derived. 2019 who assumed that female fitness increases with number of matings). Therefore, our model did not account for any genetic variation in the mating pattern and it was not necessary to specify its genetic basis to investigate its expected effect on the current barrier to gene flow. analysed the data. Young animals with spiral ridges may be confused with Littorina saxatilis. After filtering out individuals with more than 50% missing data (fewer than 40 genotypes), we were left with 3145 individuals with an average of 5.9% missing data. Littorina saxatilis (Olivi, 1792) is an intermediate host for 12 species of trematodes belonging to eight families, they all cause parasitic castration of the infected snails. (b) Estimates of FST between sample locations, both within and between L. arcana and L. saxatilis. To date, most studies of speciation in L. saxatilis have focused on the parallel evolution of RI between locally adapted ‘crab’ and ‘wave’ ecotypes owing to divergent selection in different areas of the intertidal zone [17,18,20,33,34]. Size‐assortative mating acts as a barrier to gene flow when the probability of mating between two populations of different sizes is reduced. If the trait is also under natural selection and the ecological optima differ between populations, the stabilizing sexual selection may oppose divergence, but it can also contribute to reproductive isolation once divergence is achieved. Figure S2. This is likely to result in sexual size dimorphism, which is commonly observed in marine gastropods (Ng et al. After generating virtual mating encounters using a custom script, we computed, for each position along the transect on a specific island, the correlation (Pearson's r) between female and male ln(size) in the virtual mated pairs (i.e., assortative mating) and the difference in mean and variance of ln(size) of mated males compared to all the males that were generated at that particular transect position (i.e., sexual selection). The square of the size ratio was expected to account for most of the variance because alone it would generate a decrease in mating probability on either side of a size ratio of zero (i.e., equal size male and female). Littorina arcana shows parallel ecotypic variation to L. saxatilis at some sites [24]. One thousand simulated F1s were generated by randomly intercrossing individuals from each mode using the observed genotypes. In models of parapatric speciation, coupling occurs when multiple isolating traits are subject to divergent selection on opposite sides of a sharp ecological boundary [12,13]. 2011; Servedio and Hermisson 2019). A component of sexual selection can enhance the barrier effect, even if it is not divergent. Samples were returned to the University of Sheffield and dissected to identify sex, reproductive status and reproductive mode according to Reid [24]. “Reference” snails (used as mating partners, see below) were sampled at a fifth island (“ANG” in Westram et al. The difference was driven mainly by France, where L. arcana was roughly three times more common than L. saxatilis. We inferred the historical pattern of gene flow between L. arcana and L. saxatilis by fitting demographic models to the JSFS using a version of the program ∂a∂i [31] that includes an improved optimization method and the ability to model semipermeable migration across the genome [32]. Evolutionary relationships between Littorina arcana (egg-laying) and Littorina saxatilis (brooding). Although it is important to acknowledge that violations of our simple model (e.g. Consistent with levels of FST, separation on PC1 was largest in England and smallest in France. We estimated a hybrid index across all loci (i.e., both those influencing male and those influencing female size). However, mating patterns can also impede divergence (Servedio and Hermisson 2019). S1; for further sampling details, see Westram et al. However, other barriers, including assortative mating and microhabitat choice, may also play important roles, or may even be the primary barrier to gene flow. The relationship between probability of mating (, The observed mating pattern reflected the extent of assortative mating, displacement of the optimum size ratio from zero (i.e., from equal male and female sizes), and asymmetry of the mating function. Thus, size is a multiple‐effect trait, under direct divergent selection between the Crab and Wave habitats and also a key trait influencing mating success. Because sexual selection can contribute to the barrier to gene flow, this is important. The evolution of strong reproductive isolation between sympatric intertidal snails, Akaike information criterion (AIC) for nine demographic models fitted to JSFS for each location using, Parameter estimates from the best-fitting demographic model (IM2R82, Degree of sympatry affects reinforcement in, Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement, Divergent outcomes of reinforcement speciation: the relative importance of assortative mating and migration modification, The evolution of strong reproductive isolation. Any supporting information supplied by the natural Environment Research Council ( NERC ) and in the organization execution! So that no two SNPs were within 5 KB of each other female is... Distributions may indicate that some gene flow that it generates, can also impede divergence ( cf with close!, R.K.B., Z.B.Z., T.B the link below to share a version. 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