Sampling scale can cause bias in positive assortative mating estimates: The first evidence in two intertidal snails

Assortative mating in the wild is commonly estimated by correlating between traits in mating pairs (e.g. size of males and females). Unfortunately such an approach may suffer from considerable sampling bias when the distribution of different expressions of a trait in the wild is non-random; for example, when segregation of different size classes of individuals occur in different microhabitats or areas. Consequently, any observed trait correlation in the wild can be an artifact of pooling heterogeneous samples of mating pairs from different microhabitats or areas rather than true non-random matings. This bias in estimating trait correlations due to sampling scale is termed the scale-of-choice effect (SCE). Here we use two intertidal littorinid species from Hong Kong to show how the SCE can bias size-assortative mating estimates from mating pairs captured in the wild, empirically demonstrating the influence of this effect on measures of positive assortative mating. This finding cautions that studies that have overlooked SCE may have misinterpreted the magnitude and the cause of assortative mating, and we provide a new analytical approach to protect against this potential bias in future studies

The causal relationship between sexual selection and sexual size dimorphism in marine gastropods

Sexual size dimorphism is widespread among dioecious species, but its underlying driving forces are often complex. A review of sexual size dimorphism in marine gastropods revealed two common patterns: first, sexual size dimorphism, with females being larger than males, and, second, females being larger than males in mating pairs. Both patterns suggest sexual selection and sexual size dimorphism are causally related. To test this hypothesis, we investigated, first, mechanisms driving sexual selection on size in three congeneric marine gastropods with different degrees of sexual size dimorphism, and, second, the correlation between male/female sexual selection and sexual size dimorphism across several marine gastropod species. Male mate choice via mucus trail following (as evidence of sexual selection) was found during the mating process in all three congeneric species, even though not all species showed sexual size dimorphism. There was also a significant and strong negative correlation between female sexual selection and sexual size dimorphism across 16 cases from seven marine gastropod species. These results suggest that sexual selection does not drive sexual size dimorphism. There was, however, evidence of males utilizing a similar mechanism to choose mates (i.e. selecting a female slightly larger than their own size) which may be widespread among gastropods, and, in tandem with sexual size dimorphism varying between species, provides a plausible explanation of the mating patterns observed in marine gastropods

Thermodynamic effects drive countergradient responses in the thermal performance of Littorina saxatilis across latitude.

Thermal performance curves (TPCs) provide a powerful framework to assess the evolution of thermal sensitivity in populations exposed to divergent selection regimes across latitude. However, there is a lack of consensus regarding the extent to which physiological adjustments that compensate for latitudinal temperature variation (metabolic cold adaptation; MCA) may alter the shape of TPCs, including potential repercussion on upper thermal limits. To address this, we compared TPCs for cardiac activity in latitudinally-separated populations of the intertidal periwinkle Littorina saxatilis. We applied a non-linear TPC modelling approach to explore how different metrics governing the shape of TPCs varied systematically in response to local adaptation and thermal acclimation. Both critical upper limits, and the temperatures at which cardiac performance was maximised, were higher in the northernmost (cold-adapted) population and displayed a countergradient latitudinal trend which was most pronounced following acclimation to low temperatures. We interpret this response as a knock-on consequence of increased standard metabolic rate in high latitude populations, indicating that physiological compensation associated with MCA may indirectly influence variation in upper thermal limits across latitude. Our study highlights the danger of assuming that variation in any one aspect of the TPC is adaptive without appropriate mechanistic and ecological context

Adaptive Traits Are Maintained on Steep Selective Gradients despite Gene Flow and Hybridization in the Intertidal Zone

Gene flow among hybridizing species with incomplete reproductive barriers blurs species boundaries, while selection under heterogeneous local ecological conditions or along strong gradients may counteract this tendency. Congeneric, externally-fertilizing fucoid brown algae occur as distinct morphotypes along intertidal exposure gradients despite gene flow. Combining analyses of genetic and phenotypic traits, we investigate the potential for physiological resilience to emersion stressors to act as an isolating mechanism in the face of gene flow. Along vertical exposure gradients in the intertidal zone of Northern Portugal and Northwest France, the mid-low shore species Fucus vesiculosus, the upper shore species Fucus spiralis, and an intermediate distinctive morphotype of F. spiralis var. platycarpus were morphologically characterized. Two diagnostic microsatellite loci recovered 3 genetic clusters consistent with prior morphological assignment. Phylogenetic analysis based on single nucleotide polymorphisms in 14 protein coding regions unambiguously resolved 3 clades; sympatric F. vesiculosus, F. spiralis, and the allopatric (in southern Iberia) population of F. spiralis var. platycarpus. In contrast, the sympatric F. spiralis var. platycarpus (from Northern Portugal) was distributed across the 3 clades, strongly suggesting hybridization/introgression with both other entities. Common garden experiments showed that physiological resilience following exposure to desiccation/heat stress differed significantly between the 3 sympatric genetic taxa; consistent with their respective vertical distribution on steep environmental clines in exposure time. Phylogenetic analyses indicate that F. spiralis var. platycarpus is a distinct entity in allopatry, but that extensive gene flow occurs with both higher and lower shore species in sympatry. Experimental results suggest that strong selection on physiological traits across steep intertidal exposure gradients acts to maintain the 3 distinct genetic and morphological taxa within their preferred vertical distribution ranges. On the strength of distributional, genetic, physiological and morphological differences, we propose elevation of F. spiralis var. platycarpus from variety to species level, as F. guiryi

Selection on hybrids of ecologically divergent ecotypes of a marine snail The relative importance of exogenous and endogenous barriers

Unravelling the form of selection acting on hybrids of ecotypes undergoing ecological speciation is essential to understand the mechanisms behind the evolution of reproductive isolation in the face of gene flow. Shell phenotype is known to be affected by natural selection and is involved in the fitness of the marine snail Littorina saxatilis. Here, we studied the association between shell traits and fitness in hybrids in order to determine the relative role of exogenous and endogenous selection in this hybrid zone of L.saxatilis. We show that directional selection is the predominant mode of selection among hybrids. We also show its heterogeneity, affecting different shell traits, within populations at the level of the microhabitat. Therefore, endogenous selection mechanisms are most probably lacking in this hybrid zone and exogenous barriers (pre- and post-zygotic) are possibly one of the main forces behind the evolution of barriers to gene flow between these ecologically divergent ecotypes. This study shows how this barrier might represent an important type of reproductive isolation within ecological speciation, and this should be taken into account in future studies of speciation in hybrid zones

The role of local ecology during hybridization at the initial stages of ecological speciation in a marine snail

Hybrid zones of ecologically divergent populations are ideal systems to study the interaction between natural selection and gene flow during the initial stages of speciation. Here, we perform an amplified fragment length polymorphism (AFLP) genome scan in parallel hybrid zones between divergent ecotypes of the marine snail Littorina saxatilis, which is considered a model case for the study of ecological speciation. Ridged-Banded (RB) and Smooth-Unbanded (SU) ecotypes are adapted to different shore levels and microhabitats, although they present a sympatric distribution at the mid-shore where they meet and mate (partially assortatively). We used shell morphology, outlier and nonoutlier AFLP loci from RB, SU and hybrid specimens captured in sympatry to determine the level of phenotypic and genetic introgression. We found different levels of introgression at parallel hybrid zones and nonoutlier loci showed more gene flow with greater phenotypic introgression. These results were independent from the phylogeography of the studied populations, but not from the local ecological conditions. Genetic variation at outlier loci was highly correlated with phenotypic variation. In addition, we used the relationship between genetic and phenotypic variation to estimate the heritability of morphological traits and to identify potential Quantitative Trait Loci to be confirmed in future crosses. These results suggest that ecology (exogenous selection) plays an important role in this hybrid zone. Thus, ecologically based divergent natural selection is responsible, simultaneously, for both ecotype divergence and hybridization. On the other hand, genetic introgression occurs only at neutral loci (nonoutliers). In the future, genome-wide studies and controlled crosses would give more valuable information about this process of speciation in the face of gene flow. © 2013 European Society For Evolutionary Biology

Genetic differentiation and estimation of effective population size and migration rates in two sympatric ecotypes of the marine snail Littorina saxatilis

On exposed rocky shores in Galicia (northwest Spain), a striking polymorphism exists between two ecotypes (RB and SU) of Littorina saxatilis that occupy different levels of the intertidal zone and exhibit an incomplete reproductive isolation. The setting has been suggested to represent ongoing sympatric speciation by ecological adaptation of the two ecotypes to their respective habitats. In this article we address whether or not the ecotypes have developed their own population structures in response to the rigors of their corresponding environments and life histories. We analyzed four to five allozymic loci from three surveys of the same sites, spanning a 14-year period. An experimental design including three localities with two transects per locality and three shore levels allowed studying temporal and spatial population structure and estimation of effective population sizes (Ne), neighborhood sizes (Nn), and migration rates (m). Genetic differentiation was significantly lower in RB populations (θST = 0.067) than in SU ones (θST = 0.124). Mean estimates of Ne, Nn, and m did not differ significantly between ecotypes, but local ecotype differences in migration between the two closest localities (larger migration rates in RB than in SU populations) could explain the pattern in population differentiation. © The American Genetic Association. 2005. All rights reserved