Sperm competition experiments reveal low prezygotic postmating isolation between parasitic and nonparasitic lamprey ecotypes.

The role of postmating sexual selection as a potential reproductive barrier in speciation is not well understood. Here, we studied the effects of sperm competition and cryptic female choice as putative postmating barriers in two lamprey ecotypes with a partial reproductive isolation. The European river lamprey Lampetra fluviatilis is anadromous and parasitic of other fish species, whereas the brook lamprey Lampetra planeri is freshwater resident and nonparasitic. We measured sperm traits in both ecotypes and designed sperm competition experiments to test the occurrence of cryptic female choice. We also performed sperm competition experiments either at equal semen volume or equal sperm number to investigate the role of sperm velocity on fertilization success. We observed distinct sperm traits between ecotypes with a higher sperm concentration and a lower sperm velocity for L. planeri compared with L. fluviatilis. The outcomes of sperm competition reflected these differences in sperm traits, and there was no evidence for cryptic female choice irrespective of female ecotype. At equal semen volume, L. planeri males had a higher fertilization success than L. fluviatilis and vice versa at equal sperm number. Our results demonstrate that different sperm traits between ecotypes can influence the male reproductive success and thus gene flow between L. planeri and L. fluviatilis. However, postmating prezygotic barriers are absent and thus cannot explain the partial reproductive isolation between ecotypes.

A SNP marker to discriminate the european brook lamprey (Lampetra planeri), river lamprey (L. fluviatilis) and their hybrids.

BACKGROUND: The European River lamprey Lampetra fluviatilis and the brook lamprey L. planeri are two closely related species that are also considered as partially reproductively isolated ecotypes. At the larval stage, they cannot be distinguished morphologically or genetically by mitochondrial DNA. We aimed at developing a molecular tool to identify early life stages of L. fluviatilis and L. planeri. METHODS AND RESULTS: We first identified Single Nucleotide Polymorphism (SNP) markers with distinct alleles between L. fluviatilis and L. planeri based on RADseq data from 186 individuals collected in France. Then, we developed a quantitative PCR protocol to genotype a species-specific SNP, which was tested on 270 samples including larvae and adults from both species and 17 sites from Western Europe. Results were consistent with morphological identification in all cases except for samples from the Rhône drainage and the Loch Lomond in Scotland. CONCLUSIONS: This marker allows the identification of larval stages of L. fluviatilis, L. planeri as well as hybrids. The two cases where the marker was not diagnostic might be explained by an isolated and distinct L. planeri lineage in the Rhône drainage, and high levels of admixture among L. fluviatilis, L. planeri and the lake-parasitic form in Loch Lomond.

Cytidine deaminase 2 is required for VLRB antibody gene assembly in lampreys.

The antibodies of jawless vertebrates consist of leucine-rich repeat arrays encoded by somatically assembled VLRB genes. It is unknown how the incomplete germline VLRB loci are converted into functional antibody genes during B lymphocyte development in lampreys. In Lampetra planeri larvae lacking the cytidine deaminase CDA2 gene, VLRB assembly fails, whereas the T lineage-associated VLRA and VLRC antigen receptor gene assemblies occur normally. Thus, CDA2 acts in a B cell lineage-specific fashion to support the somatic diversification of VLRB antibody genes. CDA2 is closely related to activation-induced cytidine deaminase (AID), which is essential for the elaboration of immunoglobulin gene repertoires in jawed vertebrates. Our results thus identify a convergent mechanism of antigen receptor gene assembly and diversification that independently evolved in the two sister branches of vertebrates.

Genomic and geographic footprints of differential introgression between two divergent fish species (Solea spp.).

Investigating gene flow between closely related species and its variation across the genome is important to understand how reproductive barriers shape genome divergence before speciation is complete. An efficient way to characterize differential gene flow is to study how the genetic interactions that take place in hybrid zones selectively filter gene exchange between species, leading to heterogeneous genome divergence. In the present study, genome-wide divergence and introgression patterns were investigated between two sole species, Solea senegalensis and Solea aegyptiaca, using restriction-associated DNA sequencing (RAD-Seq) to analyze samples taken from a transect spanning the hybrid zone. An integrative approach combining geographic and genomic clines methods with an analysis of individual locus introgression accounting for the demographic history of divergence was conducted. Our results showed that the two sole species have come into secondary contact postglacially, after experiencing a prolonged period (ca. 1.1 to 1.8 Myrs) of allopatric separation. Secondary contact resulted in the formation of a tension zone characterized by strong reproductive isolation, which only allowed introgression in a limited fraction of the genome. We found multiple evidence for a preferential direction of introgression in the S. aegyptiaca genetic background, indicating a possible recent or ongoing movement of the hybrid zone. Deviant introgression signals found in the opposite direction suggested that S. senegalensis could have possibly undergone adaptive introgression that has not yet spread throughout the entire species range. Our study thus illustrates the varied outcomes of genetic interactions between divergent gene pools that recently met after a long history of divergence.

Introgressive hybridization and morphological transgression in the contact zone between two Mediterranean Solea species.

Hybrid zones provide natural experiments where new combinations of genotypes and phenotypes are produced. Studying the reshuffling of genotypes and remodeling of phenotypes in these zones is of particular interest to document the building of reproductive isolation and the possible emergence of transgressive phenotypes that can be a source of evolutionary novelties. Here, we specifically investigate the morphological variation patterns associated with introgressive hybridization between two species of sole, Solea senegalensis and Solea aegyptiaca. The relationship between genetic composition at nuclear loci and individual body shape variation was studied in four populations sampled across the hybrid zone located in northern Tunisia. A strong correlation between genetic and phenotypic variation was observed among all individuals but not within populations, including the two most admixed ones. Morphological convergence between parental species was observed close to the contact zone. Nevertheless, the samples taken closest to the hybrid zone also displayed deviant segregation of genotypes and phenotypes, as well as transgressive phenotypes. In these samples, deviant body shape variation could be partly attributed to a reduced condition index, and the distorted genetic composition was most likely due to missing allelic combinations. These results were interpreted as an indication of hybrid breakdown, which likely contributes to postmating reproductive isolation between the two species.

Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era.

Estimating the rate of exchange of individuals among populations is a central concern to evolutionary ecology and its applications to conservation and management. For instance, the efficiency of protected areas in sustaining locally endangered populations and ecosystems depends on reserve network connectivity. The population genetics theory offers a powerful framework for estimating dispersal distances and migration rates from molecular data. In the marine realm, however, decades of molecular studies have met limited success in inferring genetic connectivity, due to the frequent lack of spatial genetic structure in species exhibiting high fecundity and dispersal capabilities. This is especially true within biogeographic regions bounded by well-known hotspots of genetic differentiation. Here, we provide an overview of the current methods for estimating genetic connectivity using molecular markers and propose several directions for improving existing approaches using large population genomic datasets. We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples. We then focus on alternative methods based on markers influenced by selection. Although some of these methodologies are still underexplored, our aim was to stimulate new research to test how broadly they are applicable to nonmodel marine species. We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally. We finally present how neutral markers hitchhiking with selected loci can also provide information about connectivity patterns within apparently well-mixed biogeographic regions. We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.