Genetic structure and signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos)

Abstract

With overfishing reducing the abundance of marine predators in multiple marine ecosystems, knowledge of genetic structure and local adaptation may provide valuable information to assist sustainable management. Despite recent technological advances, most studies on sharks have used small sets of neutral markers to describe their genetic structure. We used 5517 nuclear single-nucleotide polymorphisms (SNPs) and a mitochondrial DNA (mtDNA) gene to characterize patterns of genetic structure and detect signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos). Using samples from Australia, Indonesia and oceanic reefs in the Indian Ocean, we established that large oceanic distances represent barriers to gene flow, whereas genetic differentiation on continental shelves follows an isolation by distance model. In Australia and Indonesia differentiation at nuclear SNPs was weak, with coral reefs acting as stepping stones maintaining connectivity across large distances. Differentiation of mtDNA was stronger, and more pronounced in females, suggesting sex-biased dispersal. Four independent tests identified a set of loci putatively under selection, indicating that grey reef sharks in eastern Australia are likely under different selective pressures to those in western Australia and Indonesia. Genetic distances averaged across all loci were uncorrelated with genetic distances calculated from outlier loci, supporting the conclusion that different processes underpin genetic divergence in these two data sets. This pattern of heterogeneous genomic differentiation, suggestive of local adaptation, has implications for the conservation of grey reef sharks; furthermore, it highlights that marine species showing little genetic differentiation at neutral loci may exhibit patterns of cryptic genetic structure driven by local selection.

Evidence for rapid recovery of shark populations within a coral reef marine protected area

“…Additionally, tracking studies at isolated reefs both in the same region (Rowley Shoals) and elsewhere in tropical Australia have shown that C. amblyrhynchos adults tend to be resident over protracted time frames (months -years) (Barnett et al 2012;Espinoza et al 2015;Field et al 2011). This is confirmed by a recent genetic study that has shown that populations of C. amblyrhynchos on the Rowley Shoals and the Scott Reefs are likely to be largely self-recruiting and demographically independent (Momigliano et al 2017). Although the proximity of other reefs and shoals to the east of Ashmore Reef may still increase the likelihood of immigration, this might have been counteracted by the prevalence of illegal fishing in the Australian Exclusive Economic Zone (EEZ), which has severely reduced shark numbers on reefs and shoals across a wide portion of the region surrounding Ashmore (Field et al 2009).…”

Weak population structure of the Spot‐tail shark Carcharhinus sorrah and the Blacktip shark C. limbatus along the coasts of the Arabian Peninsula, Pakistan, and South Africa

“…In particular, the offspring of C. limbatus migrates from nursery grounds to offshore wintering grounds when temperatures drop below 21°C (Castro, 1996). This Future research to understand the role of philopatric behavior in generating fine-scale structure in shark populations (Momigliano et al, 2017;Pazmiño et al, 2018;Portnoy et al, 2015) in the Arabian region is warranted. Particular focus should be placed on a comparison of geographic scales of heterogeneity partition produced by neutral (both microsatellite and mtDNA) vs. non-neutral markers.…”

Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper (Phaulacridium vittatum)

“…High gene flow between populations may interfere with local adaptation by homogenizing locally adapted genotypes and alleles under weak selection (Antonovics, ; Lenormand, ; Yeaman & Whitlock, ). However, the establishment and maintenance of local adaptation also depends on the introduction of novel genetic variation on which selection can act (Fitzpatrick, Gerberich, Kronenberger, Angeloni, & Funk, ; Kawecki & Ebert, ; Tigano & Friesen, ), and local adaptation may still occur under the neutralizing effects of high gene flow (e.g., birds: Attard et al, ; trees: Gonzalo‐Turpin & Hazard, ; sharks: Momigliano et al, ; frogs: Muir, Biek, Thomas, & Mable, ). Despite expectations that high genetic connectivity limits selection on adaptive loci within populations (Barton & Partridge, ; Kawecki & Ebert, ; Rasanen & Hendry, ), what we know about the interplay between gene flow and local adaptation remains varied and inconsistent (Savolainen, Lascoux, & Merila, ).…”