Targeted Sequencing of Mitochondrial Genes Reveals Signatures of Molecular Adaptation in a Nearly Panmictic Small Pelagic Fish Species

Abstract

Ongoing climatic changes, with predictable impacts on marine environmental conditions, are expected to trigger organismal responses. Recent evidence shows that, in some marine species, variation in mitochondrial genes involved in the aerobic conversion of oxygen into ATP at the cellular level correlate with gradients of sea surface temperature and gradients of dissolved oxygen. Here, we investigated the adaptive potential of the European sardine Sardina pilchardus populations offshore the Iberian Peninsula. We performed a seascape genetics approach that consisted of the high throughput sequencing of mitochondria’s ATP6, COI, CYTB and ND5 and five microsatellite loci on 96 individuals coupled with environmental information on sea surface temperature and dissolved oxygen across five sampling locations. Results show that, despite sardines forming a nearly panmictic population around Iberian Peninsula, haplotype frequency distribution can be explained by gradients of minimum sea surface temperature and dissolved oxygen. We further identified that the frequencies of the most common CYTB and ATP6 haplotypes negatively correlate with minimum sea surface temperature across the sampled area, suggestive of a signature of selection. With signatures of selection superimposed on highly connected populations, sardines may be able to follow environmental optima and shift their distribution northwards as a response to the increasing sea surface temperatures.

Evidence for Selection on Mitochondrial OXPHOS Genes in the Mediterranean Killifish Aphanius fasciatus Valenciennes, 1821

“…It has also been hypothesized that the interaction between positively selected sites of COX subunits could affect enzyme regulation and OXPHOS efficiency in Istiophoridae, a family of highly aerobic fish [48]. A signature of positive or directional selection was found in three sites of Cytb in Sardina pilchardus populations, and a correlation between the most frequent Cytb haplotype and the minimum sea surface temperature was detected [49]. Interestingly, the mitochondrial performance of the heart and brain, following thermal acclimation to extreme temperatures, in locally adapted subspecies of the Atlantic killifish Fundulus heteroclitus, highlighted a complex mitochondrial regulation in this deeply eurythermal species, with OXPHOS efficiency and reactive oxygen dynamics probably playing a pivotal role in thermal acclimation and local adaptation [50].…”

Sardines at a junction: Seascape genomics reveals ecological and oceanographic drivers of variation in the NW Mediterranean Sea

“…Its hydrological characteristics are closer to those of the Northeastern Atlantic than to the Western Mediterranean (Bacha et al, 2014), indicative of enhanced gene flow between the Alboran Sea and the Atlantic (Northeast and Moroccan Atlantic Ocean, Baibai et al, 2012). The AOF constitutes a barrier to sardine dispersal that could be held responsible for founder effects, followed by genetic drift with selection acting on the local scale driving adaptations mostly related to minimum sea surface temperature (Baltazar‐Soares et al, 2021). The AOF as a barrier that separates the Atlantic and the Mediterranean is commonly observed in other fish species, such as Sardinella aurita , Mugil cephalus and Xiphias gladius (Borsa et al, 1997); Merluccius merluccius (Lundy et al, 1999); three sparid species, Lithognatus mormyrus , Spondyliosoma cantharus and Dentex dentex (Bargelloni et al, 2003); horse mackerel ( Trachurus trachurus ) populations (Abaunza et al, 2008) and Dicentrarchus labrax (Naciri et al, 1999).…”

Towards a unified eco-evolutionary framework for fisheries management: Coupling advances in next-generation sequencing with species distribution modelling

“…Early implementations of genetic information came tackle some of the wider gaps on fisheries management, such as estimates of stock connectivity and delimitation, development of monitoring programs, and design of marine protected areas (Hauser and Carvalho, 2008;Verspoor et al, 2008;Casey et al, 2016;Blasco et al, 2020). Characterizing genetic diversity as respective distribution patterns became more enticing with NGS as it permitted to expand the search beyond the traditional stock structure and connectivity towards signatures of selection and inference of the putative adaptive potential of those same stocks (Therkildsen et al, 2013;Baltazar-Soares et al, 2021b). Inferring adaptive potential on top of stock connectivity is pivotal to estimate the repertoire of genetic-based adaptive responses and build expectations on the spatial reshuffling of adaptive alleles (Eizaguirre and Baltazar-Soares, 2014;Capblancq et al, 2020).…”