Population genomic response to geographic gradients by widespread and endemic fishes of the Arabian Peninsula

Abstract

Genetic structure within marine species may be driven by local adaptation to their environment, or alternatively by historical processes, such as geographic isolation.The gulfs and seas bordering the Arabian Peninsula offer an ideal setting to examine connectivity patterns in coral reef fishes with respect to environmental gradients and vicariance. The Red Sea is characterized by a unique marine fauna, historical periods of desiccation and isolation, as well as environmental gradients in salinity, temperature, and primary productivity that vary both by latitude and by season. The adjacent Arabian Sea is characterized by a sharper environmental gradient, ranging from extensive coral cover and warm temperatures in the southwest, to sparse coral cover, cooler temperatures, and seasonal upwelling in the northeast. Reef fish, however, are not confined to these seas, with some Red Sea fishes extending varying distances into the northern Arabian Sea, while their pelagic larvae are presumably capable of much greater dispersal. These species must therefore cope with a diversity of conditions that invoke the possibility of steep clines in natural selection. Here, we test for genetic structure in two widespread reef fish species (a butterflyfish and surgeonfish) and eight range-restricted butterflyfishes across the Red Sea and Arabian Sea using genome-wide single nucleotide polymorphisms. We performed multiple matrix regression with randomization analyses on genetic distances for all species, as well as reconstructed scenarios for population subdivision in the species with signatures of isolation. We found that (a) widespread species displayed more genetic subdivision than regional endemics and (b) this genetic structure was not correlated with contemporary environmental parameters but instead may reflect historical events. We propose that the endemic species may be adapted to a diversity of local conditions, but the widespread species are instead subject to ecological filtering where different combinations of genotypes persist under divergent ecological regimes. | 4315 DIBATTISTA eT Al.

Andean and California condors possess dissimilar genetic composition but exhibit similar demographic histories

“…Nevertheless, long‐term effects of translocations have been rarely assessed, and findings are inconsistent across systems: Some translocations have succeeded in increasing population fitness by incorporating new alleles (Johnson et al., 2010; Whiteley et al., 2015), while others have failed by underestimating the negative effects of genetic homogenization, outbreeding depression, disease transmissions or behavioral divergence (e.g., Deredec & Courchamp, 2007; Grauer et al., 2017; Kock et al., 2010; Manlick et al., 2017). This points to the importance of considering the natural history of populations in management plans, especially when species are geographically widespread as they may exhibit considerable differences in the degree of adaptation, isolation, and gene flow, resulting in possible incompatible genetic traits (DiBattista et al., 2020; Moritz, 1999).…”

“…underestimating the negative effects of genetic homogenization, outbreeding depression, disease transmissions or behavioral divergence (e.g., Deredec & Courchamp, 2007;Grauer et al, 2017;Kock et al, 2010;Manlick et al, 2017). This points to the importance of considering the natural history of populations in management plans, especially when species are geographically widespread as they may exhibit considerable differences in the degree of adaptation, isolation, and gene flow, resulting in possible incompatible genetic traits (DiBattista et al, 2020;Moritz, 1999).…”

Physical-biological interactions underlying the phylogeographic patterns of coral-dependent fishes around the Arabian Peninsula

“…Investigations performed hitherto have not showed genetic discontinuities of species through the Bab el-Mandeb Strait, including fishes A. bicinctus (Saenz-Agudelo et al, 2015); C. hemistiktos (Priest et al 2016); P. maculosus (Torquato et al, 201); Chaetodon spp. (DiBattista et al, 2020) and sea anemones (Emms et al, 2019). In fact, the strength of the barrier has been mainly debated based on the species distribution studies.…”

Natural experiments and long-term monitoring are critical to understand and predict marine host–microbe ecology and evolution

“…The narrow Strait of Bab al Mandab connects the warm and saline semi-enclosed Red Sea with the open and more variable Arabian Sea. The Red Sea is host to many endemic species (5% to 13% endemic across a range of taxa [ 67 ]), while the pronounced seasonal variations in the Arabian Sea have driven fine-scale local adaptations [ 68 ]. Although the Mediterranean has been connected to the Atlantic through the Strait of Gibraltar since the end of the Messinian Salinity Crisis 5.3 Ma [ 69 ], the modern Mediterranean fauna bears the more recent imprint of Pleistocene glacial and interglacial cycles.…”