Positive selection on sperm ion channels in a brooding brittle star: consequence of life‐history traits evolution

Abstract

Closely related species are key models to investigate mechanisms leading to reproductive isolation and early stages of diversification, also at the genomic level. The brittle star cryptic species complex Ophioderma longicauda encompasses the sympatric broadcast-spawning species C3 and the internal brooding species C5. Here, we used de novo transcriptome sequencing and assembly in two closely related species displaying contrasting reproductive modes to compare their genetic diversity and to investigate the role of natural selection in reproductive isolation. We reconstructed 20 146 and 22 123 genes for C3 and C5, respectively, and characterized a set of 12 229 orthologs. Genetic diversity was 1.5-2 times higher in C3 compared to C5, confirming that species with low parental investment display higher levels of genetic diversity. Forty-eight genes were the targets of positive diversifying selection during the evolution of the two species. Notably, two genes (NHE and TetraKCNG) are sperm-specific ion channels involved in sperm motility. Ancestral sequence reconstructions show that natural selection targeted the two genes in the brooding species. This may result from an adaptation to the novel environmental conditions surrounding sperm in the brooding species, either directly affecting sperm or via an increase in male/female conflict. This phenomenon could have promoted prezygotic reproductive isolation between C3 and C5. Finally, the sperm receptors to egg chemoattractants differed between C3 and C5 in the ligand-binding region. We propose that mechanisms of species-specific gamete recognition in brittle stars occur during sperm chemotaxis (sperm attraction towards the eggs), contrary to other marine invertebrates where prezygotic barriers to interspecific hybridization typically occur before sperm-egg fusion.

Persistent postmating, prezygotic reproductive isolation between populations

“…Postmating, prezygotic isolation in external fertilizers is mostly limited to incompatibilities relating to chemo-attraction between gametes (Weber et al, 2017) and/or gamete interactions at the cell surface (Vacquier & Swanson, 2011). For internal fertilizers, an additional array of potential PMPZ reproductive barriers can act as a result of the complex series of events that take place within the female reproductive tract after mating (Bloch Qazi, Heifetz, & Wolfner, 2003;Orr & Brennan, 2015;Schnakenberg, Siegal, & Bloch Qazi, 2012).…”

Problems and Questions Posed by Cryptic Species. A Framework to Guide Future Studies

“…Because humans use visual information for nominal species delimitation, animals that use visual cues for mate recognition (such as vertebrates) are also much less likely to form CGI than animals that rely entirely on chemical cues for mating, such as marine invertebrates (e.g. spawning is generally triggered by chemical signals, and gametes from both sexes themselves are attracted by chemical signals (Weber et al 2017)). Tiny organisms provide fewer characters that can be used for diagnosis, parasites often have lost many morphological characters with respect to their free-living relatives, because their bodies are simplified, having lost some major functions, etc.…”

Species delimitation in the presence of strong incomplete lineage sorting and hybridization: lessons fromOphioderma(Ophiuroidea: Echinodermata)

“…Extracted DNA was diluted 10x in sterile water prior to PCR. We used orthologous genes from transcriptomes of O. longicauda C3 and C5, corresponding to mitochondrial lineages L1 and L3, respectively (Weber et al, 2017(Weber et al, , 2015 to develop 55 primer pairs to test. The criteria for marker development were: (i) the marker should be polymorphic; (ii) in half of the markers, at least one diagnostic SNP between C3 and C5 should be present; (iii) the length of the PCR product should be 300-400 bp (due to sequencing technology limitations).…”