A developmentally descriptive method for quantifying shape in gastropod shells

The growth of snail shells can be described by simple mathematical rules. Variation in a few parameters can explain much of the diversity of shell shapes seen in nature. However, empirical studies of gastropod shell shape variation typically use geometric morphometric approaches, which do not capture this growth pattern. We have developed a way to infer a set of developmentally descriptive shape parameters based on three-dimensional logarithmic helicospiral growth and using landmarks from two-dimensional shell images as input. We demonstrate the utility of this approach, and compare it to the geometric morphometric approach, using a large set of Littorina saxatilis shells in which locally adapted populations differ in shape. Our method can be modified easily to make it applicable to a wide range of shell forms, which would allow for investigations of the similarities and differences between and within many different species of gastropods

The evolution of strong reproductive isolation between sympatric intertidal snails

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. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'

Spatial Distribution of Cryptic Species Diversity in European Freshwater Amphipods (Gammarus fossarum) as Revealed by Pyrosequencing

In order to understand and protect ecosystems, local gene pools need to be evaluated with respect to their uniqueness. Cryptic species present a challenge in this context because their presence, if unrecognized, may lead to serious misjudgement of the distribution of evolutionarily distinct genetic entities. In this study, we describe the current geographical distribution of cryptic species of the ecologically important stream amphipod Gammarus fossarum (types A, B and C). We use a novel pyrosequencing assay for molecular species identification and survey 62 populations in Switzerland, plus several populations in Germany and eastern France. In addition, we compile data from previous publications (mainly Germany). A clear transition is observed from type A in the east (Danube and Po drainages) to types B and, more rarely, C in the west (Meuse, Rhone, and four smaller French river systems). Within the Rhine drainage, the cryptic species meet in a contact zone which spans the entire G. fossarum distribution range from north to south. This large-scale geographical sorting indicates that types A and B persisted in separate refugia during Pleistocene glaciations. Within the contact zone, the species rarely co-occur at the same site, suggesting that ecological processes may preclude long-term coexistence. The clear phylogeographical signal observed in this study implies that, in many parts of Europe, only one of the cryptic species is present

Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize

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

Inversions and Evolution

Inversions are chromosomal rearrangements where the order of genes is reversed. Inversions originate by mutation and can be under positive, negative or balancing selection. Selective effects result from potential disruptive effects on meiosis, gene disruption at inversion breakpoints and, importantly, the effects of inversions as modifiers of recombination rate: Recombination is strongly reduced in individuals heterozygous for an inversion, allowing for alleles at different loci to be inherited as a ‘block’. This may lead to a selective advantage whenever it is favourable to keep certain combinations of alleles associated, for example under local adaptation with gene flow. Inversions can cover a considerable part of a chromosome and contain numerous loci under different selection pressures, so that the resulting overall effects may be complex. Empirical data from various systems show that inversions may have a prominent role in local adaptation, speciation, parallel evolution, the maintenance of polymorphism and sex chromosome evolution

Data from: Targeted resequencing reveals geographical patterns of differentiation for loci implicated in parallel evolution

Parallel divergence and speciation provide evidence for the role of divergent selection in generating biological diversity. Recent studies indicate that parallel phenotypic divergence may not have the same genetic basis in different geographical locations - “outlier loci” (loci potentially affected by divergent selection) are often not shared among parallel instances of phenotypic divergence. However, limited sharing may be due, in part, to technical issues if false positive outliers occur. Here, we test this idea in the marine snail Littorina saxatilis, which has evolved two partly isolated ecotypes (adapted to crab predation vs. wave action) in multiple locations independently. We argue that if the low extent of sharing observed in earlier studies in this system is due to sampling effects, we expect outliers not to show elevated FST when sequenced in new samples from the original locations, and also not to follow predictable geographical patterns of elevated FST. Following a hierarchical sampling design (within vs. between country), we applied capture sequencing, targeting outliers from earlier studies and control loci. We found that outliers again showed elevated levels of FST in their original location, suggesting they were not generated by sampling effects. Outliers were also likely to show increased FST in geographically close locations, which may be explained by higher levels of gene flow or shared ancestral genetic variation compared to more distant locations. However, in contrast to earlier findings, we also found some outlier types to show elevated FST in geographically distant locations. We discuss possible explanations for this unexpected result

What is reproductive isolation?

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

Reproductive isolation, speciation, and the value of disagreement: A reply to the commentaries on ‘What is reproductive isolation?’

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Data from: Is embryo abortion a postzygotic barrier to gene flow between Littorina ecotypes?

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 postzygotic barriers due to selection against hybrids remains unclear. High embryo abortion rates in this species could indicate the presence of such barriers. Postzygotic 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 1011 embryos (mean 130±123) and abortion rates varied between 0 and100% (mean 12%). We described female genotypes by using a hybrid index based on hundreds of SNPs differentiated between ecotypes with which we characterised 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 postzygotic barriers contributing to ecotype divergence and the high and variable abortion rates were marginally, if at all, explained by hybrid index of females