Using replicate hybrid zones to understand the genomic basis of adaptive divergence

Combining hybrid zone analysis with genomic data is a promising approach to understanding the genomic basis of adaptive divergence. It allows for the identification of genomic regions underlying barriers to gene flow. It also provides insights into spatial patterns of allele frequency change, informing about the interplay between environmental factors, dispersal and selection. However, when only a single hybrid zone is analysed, it is difficult to separate patterns generated by selection from those resulting from chance. Therefore, it is beneficial to look for repeatable patterns across replicate hybrid zones in the same system. We applied this approach to the marine snail Littorina saxatilis, which contains two ecotypes, adapted to wave-exposed rocks vs. high-predation boulder fields. The existence of numerous hybrid zones between ecotypes offered the opportunity to test for the repeatability of genomic architectures and spatial patterns of divergence. We sampled and phenotyped snails from seven replicate hybrid zones on the Swedish west coast and genotyped them for thousands of single nucleotide polymorphisms. Shell shape and size showed parallel clines across all zones. Many genomic regions showing steep clines and/or high differentiation were shared among hybrid zones, consistent with a common evolutionary history and extensive gene flow between zones, and supporting the importance of these regions for divergence. In particular, we found that several large putative inversions contribute to divergence in all locations. Additionally, we found evidence for consistent displacement of clines from the boulder–rock transition. Our results demonstrate patterns of spatial variation that would not be accessible without continuous spatial sampling, a large genomic data set and replicate hybrid zones.publishedVersio

Towards the completion of speciation : the evolution of reproductive isolation beyond the first barriers

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

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

Using replicate hybrid zones to understand the genomic basis of adaptive divergence

Combining hybrid zone analysis with genomic data is a promising approach to understanding the genomic basis of adaptive divergence. It allows for the identification of genomic regions underlying barriers to gene flow. It also provides insights into spatial patterns of allele frequency change, informing about the interplay between environmental factors, dispersal and selection. However, when only a single hybrid zone is analysed, it is difficult to separate patterns generated by selection from those resulting from chance. Therefore, it is beneficial to look for repeatable patterns across replicate hybrid zones in the same system. We applied this approach to the marine snail Littorina saxatilis, which contains two ecotypes, adapted to wave-exposed rocks vs. high-predation boulder fields. The existence of numerous hybrid zones between ecotypes offered the opportunity to test for the repeatability of genomic architectures and spatial patterns of divergence. We sampled and phenotyped snails from seven replicate hybrid zones on the Swedish west coast and genotyped them for thousands of single nucleotide polymorphisms. Shell shape and size showed parallel clines across all zones. Many genomic regions showing steep clines and/or high differentiation were shared among hybrid zones, consistent with a common evolutionary history and extensive gene flow between zones, and supporting the importance of these regions for divergence. In particular, we found that several large putative inversions contribute to divergence in all locations. Additionally, we found evidence for consistent displacement of clines from the boulder–rock transition. Our results demonstrate patterns of spatial variation that would not be accessible without continuous spatial sampling, a large genomic data set and replicate hybrid zones

Very short mountings are enough for sperm transfer in Littorina saxatilis

Author's accepted version (postprint).This is an Accepted Manuscript of an article published by Oxford University Press in Journal of Molluscan Studies on 22/02/2022.Available online: https://academic.oup.com/mollus/article-abstract/88/1/eyab049/6533478?redirectedFrom=fulltextacceptedVersio

Results of partial Mantel test, investigating the effect of clusters (A1.1, other A1, A2 for type A; B1, B2 for type B) on genetic differentiation when correcting for geographical distance.

1<p>***P<0.001; **P<0.01.</p

Population tree and geographical distribution of clusters for <i>G. fossarum</i> type B (FB: type A/outgroup).

<p>The tree (a) was calculated using the Neighbour Joining method; numbers at nodes indicate bootstrap support in % (1000 bootstraps). Main clusters are named and given a symbol. The same symbols are used to indicate the geographical location of the populations in the map (b). The three major European drainages sampled in this study are shown in different shadings. The border of Switzerland and delimitations of Swiss subdrainages are indicated by thick black lines. Relevant subdrainages of the Rhine in Switzerland are labelled (grey). The area referred to as “Lake Geneva region” in the text is also indicated. Names of populations showing evidence for recent bottlenecks (as indicated by the program BOTTLENECK using the infinite alleles mutation model) are underlined.</p

Population tree and geographical distribution of clusters for <i>G. fossarum</i> type A (MW: type B/outgroup).

<p>The tree (a) was calculated using the Neighbour Joining method; numbers at nodes indicate bootstrap support in % (1000 bootstraps). Main clusters are named and given a symbol. The same symbols are used to indicate the geographical location of the populations in the map (b). The three major European drainages sampled in this study are shown in different shadings. The border of Switzerland and delimitations of Swiss subdrainages are indicated by thick black lines. Relevant subdrainages of the Rhine in Switzerland are labelled (grey). None of the populations showed evidence of recent bottlenecks.</p

Results of Mantel tests conducted to test for isolation by distance (geographical distance vs. F_ST/(1-F_ST)) in the program IBDWS for the cryptic <i>Gammarus fossarum</i> species type A and B in different drainages.

1<p>“group” indicates the species and drainage included in the analysis. Two main clusters of type B were observed in the Rhine (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0069576#pone-0069576-g002" target="_blank">Fig. 2</a>). Isolation by distance was assessed only within the larger cluster, B1.</p>2<p>***P<0.001; **P<0.01; *P<0.05.</p>3<p>The regression slopes (IBD slope) and their confidence intervals (95% CI) are indicated if significantly different from zero. The slopes were significantly higher in type A (Rhine) than type B (Rhone) irrespective of the distance measure used.</p