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

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.     

Does color matter? Molecular and ecological divergence in four sympatric color morphs of a coral reef fish

Non‐sex‐linked color polymorphism is common in animals and can be maintained in populations via balancing selection or, when under diversifying selection, can promote divergence. Despite their potential importance in ecological interactions and the evolution of biodiversity, their function and the mechanisms by which these polymorphisms are maintained are still poorly understood. Here, we combine field observations with life history and molecular data to compare four sympatric color morphs of the coral reef fish Paracirrhites forsteri (family Cirrhitidae) in the central Red Sea. Our findings verify that the color morphs are not sex‐limited, inhabit the same reefs, and do not show clear signs of avoidance or aggression among them. A barcoding approach based on 1,276 bp of mitochondrial DNA could not differentiate the color morphs. However, when 36,769 SNPs were considered, we found low but significant population structure. Focusing on 1,121 F_ST outliers, we recovered distinct population clusters that corresponded to shifts in allele frequencies with each color morph harboring unique alleles. Genetic divergence at these outlier loci is accompanied by differences in growth and marginal variation in microhabitat preference. Together, life history and molecular analysis suggest subtle divergence between the color morphs in this population, the causes for which remain elusive.     

Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo‐Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea‐level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial‐scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo‐Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales.     

Persistence of self-recruitment and patterns of larval connectivity in a marine protected area network

The use of marine protected area (MPA) networks to sustain fisheries and conserve biodiversity is predicated on two critical yet rarely tested assumptions. Individual MPAs must produce sufficient larvae that settle within that reserve's boundaries to maintain local populations while simultaneously supplying larvae to other MPA nodes in the network that might otherwise suffer local extinction. Here, we use genetic parentage analysis to demonstrate that patterns of self-recruitment of two reef fishes (Amphiprion percula and Chaetodon vagabundus) in an MPA in Kimbe Bay, Papua New Guinea, were remarkably consistent over several years. However, dispersal from this reserve to two other nodes in an MPA network varied between species and through time. The stability of our estimates of self-recruitment suggests that even small MPAs may be self-sustaining. However, our results caution against applying optimization strategies to MPA network design without accounting for variable connectivity among species and over time.     

Amplified genes may be overexpressed, unchanged, or downregulated in cervical cancer cell lines

Several copy number-altered regions (CNAs) have been identified in the genome of cervical cancer, notably, amplifications of 3q and 5p. However, the contribution of copy-number alterations to cervical carcinogenesis is unresolved because genome-wide there exists a lack of correlation between copy-number alterations and gene expression. In this study, we investigated whether CNAs in the cell lines CaLo, CaSki, HeLa, and SiHa were associated with changes in gene expression. On average, 19.2% of the cell-line genomes had CNAs. However, only 2.4% comprised minimal recurrent regions (MRRs) common to all the cell lines. Whereas 3q had limited common gains (13%), 5p was entirely duplicated recurrently. Genome-wide, only 15.6% of genes located in CNAs changed gene expression; in contrast, the rate in MRRs was up to 3 times this. Chr 5p was confirmed entirely amplified by FISH; however, maximum 33.5% of the explored genes in 5p were deregulated. In 3q, this rate was 13.4%. Even in 3q26, which had 5 MRRs and 38.7% recurrently gained SNPs, the rate was only 15.1%. Interestingly, up to 19% of deregulated genes in 5p and 73% in 3q26 were downregulated, suggesting additional factors were involved in gene repression. The deregulated genes in 3q and 5p occurred in clusters, suggesting local chromatin factors may also influence gene expression. In regions amplified discontinuously, downregulated genes increased steadily as the number of amplified SNPs increased (p<0.01, Spearman's correlation). Therefore, partial gene amplification may function in silencing gene expression. Additional genes in 1q, 3q and 5p could be involved in cervical carcinogenesis, specifically in apoptosis. These include PARP1 in 1q, TNFSF10 and ECT2 in 3q and CLPTM1L, AHRR, PDCD6, and DAP in 5p. Overall, gene expression and copy-number profiles reveal factors other than gene dosage, like epigenetic or chromatin domains, may influence gene expression within the entirely amplified genome segments.     

Genetic tools link long-term demographic and life-history traits of anemonefish to their anemone hosts

The life-history traits and population dynamics of species are increasingly being attributed to the characteristics of their preferred habitats. While coral reef fish are often strongly associated with particular habitats, long-term studies establishing the demographic and life-history consequences of occupying different reef substrata are rare and no studies have monitored individuals in situ over their lifetime and determined the fate of their offspring. Here, we documented a quasi-turnover and local reproductive success for an entire population of orange clownfish (Amphiprion percula) from Kimbe Island, Papua New Guinea, by taking bi-annual samples of DNA over a 10-yr period (2003–2013). We compared demographic and life-history traits of individuals living on two host anemone species, Heteractis magnifica and Stichodactyla gigantea, including female size, adult continued presence (a proxy for relative longevity range), early post-settlement growth, the number of eggs per clutch and ‘local’ reproductive success (defined for each adult as the number of offspring returning to the natal population). Our results indicate that while the relative longevity of adults was similar on both host anemone species, females living in H. magnifica were larger than females in S. gigantea. However, despite females growing larger and producing more eggs on H. magnifica, we found that local reproductive success was significantly higher for clownfish living in S. gigantea. Life-history traits also exhibited local spatial variation, with higher local reproductive success recorded for adults living on S. gigantea on the eastern side of the island. Our findings support a ‘silver-spoon’ hypothesis that predicts individuals that are fortunate enough to recruit into good habitat and location will be rewarded with higher long-term reproductive success and will make a disproportionate contribution to population renewal.     

Genetic diversity and life-history traits of bonefish Albula spp. from the Red Sea

The management of bonefishes Albula spp. has been hindered by unresolved species distributions and a general lack of life-history information. This study provides the first genetic species identifications of Albula spp. from the northern Indian Ocean. The roundjaw bonefish Albula glossodonta was documented in the Red Sea, and the smallscale bonefish A. oligolepis was identified in the Gulf of Aden with no evidence supporting sympatry. Estimates of genetic differentiation indicate three closely related lineages of A. glossodonta in the Red Sea, Indian Ocean and Pacific Ocean (Red Sea-Pacific Ocean, F_st = 0.295; Red Sea-Seychelles, F_st = 0.193; Pacific Ocean-Seychelles, F_st = 0.141). In addition, the authors provide the first life-history information of Albula spp. in the Indian Ocean. Age-based growth models of A. glossodonta from the Red Sea demonstrated statistically significant differences compared to previously published data from the Pacific Ocean. Spawning activity during winter months was derived from gonado-somatic index values of A. glossodonta from the Red Sea and corresponded with spawning seasonality previously documented for the species in the Pacific Ocean. The results of this study aid in refining biogeographical uncertainties of Albula spp. and illustrate the importance of collecting regional growth information for subsequent management of A. glossodonta.