Complex genetic structure of a euryhaline marine fish in temporarily open/closed estuaries from the wider Gulf of Aden

Temporarily open/closed estuaries (TOCEs) are major ecosystems of the Indian Ocean coastal zones. Their functioning is tightly linked to climatic events such as monsoons and storms, and their mouth can close up for prolonged and variable periods of time, thus limiting their connectivity with the marine environment. Two types of genetic markers (i.e., mitochondrial cytochrome c oxidase I (COI) gene and microsatellites) were used to assess the genetic structure of 288 individuals of Terapon jarbua, a widely distributed fish species in the wider Gulf of Aden. Firstly, the hypothesis of panmixia was tested. Then, alternative hypotheses were investigated to explain the population genetic structure of T. jarbua: could it be shaped by (1) regional biogeographic barriers (i.e., Socotra Island vs. mainland Yemen) and/or (2) the particular functioning of TOCEs in relation to the species life cycle and particular physical ocean parameters? On one hand, the polymorphism of the COI inferred (1) a high haplotype diversity and a reduced nucleotide diversity over the whole data set and (2) a star-like shape of the haplotype network, thus suggesting a population expansion after local extinctions during the Pleistocene glaciations. On a second hand, the genotyping of eight microsatellites showed a significant genetic differentiation between T. jarbua populations in the wider Gulf of Aden (F (ST) = 0.035, p < 0.01), and thus, the panmixia hypothesis was rejected. Analyses of molecular variance results did not show any significant structure between Socotra Island and mainland Yemen and thus did not support the role of biogeographic barriers in structuring T. jarbua populations. Significant multi-locus deficits in heterozygotes at particular locations displaying high levels of F (IS) were recorded. It was suggested that a possible Wahlund effect took place in those TOCEs which could gather several cohorts of larvae stemming from different marine subpopulations over the sampled area. The present study emphasized the uniqueness of each TOCE as a potential reservoir of biodiversity and the urgent need for a better conservation program of those estuaries in the region, in order to avoid habitat fragmentation and permanent closure of those nursery areas by human activities.