Introduction
Conservation of fisheries resources relies on the assessment and management of self-sustaining units called stocks, whose delimitation often oversimplifies species population dynamics (Begg et al. 1999, Stephenson 1999, Reiss et al. 2009). Yet, failing to account for stock complexity can induce overfishing and ultimately result in fisheries collapse (Hutchinson 2008), highlighting the importance of integrating knowledge on spatial structure and connectivity into management plan development processes (Kerr et al. 2016). In this context, the potential of genomic approaches is increasingly being harnessed to tackle a diverse range of fisheries management related questions, such as assessment of population structure, connectivity and adaptation to local environments (Ovenden et al. 2015, Bernatchez et al. 2017), even when genetic differentiation is low, as observed in highly migratory fish like striped marlin (Mamoozadeh et al. 2020), blue shark (Nikolic et al. 2023) and yellowfin tuna (Barth et al. 2017b). In particular, the preservation of fish genetic diversity and conservation of locally adapted populations has gained importance in the face of rapid environmental changes and increasing fishing pressure (Bonanomi et al. 2015). Species resilience may depend on adaptive evolution capacities (Hoffmann and Sgrò 2011, Bernatchez 2016), making essential the inclusion of adaptive variation in genomic studies focusing on managed species (Fraser and Bernatchez 2001, Valenzuela-Quiñonez 2016, Xuereb et al. 2021).
The Atlantic bluefin tuna (ABFT, Thunnus thynnus ) is a large and emblematic highly migratory species that inhabits waters of the North Atlantic Ocean and adjacent seas (Fromentin and Powers 2005, Collette et al. 2011). ABFT has been heavily exploited for millennia and the emergence of the sushi-sashimi market in the 1980s turned it into one of the most valuable tuna species in the international fish trade (Fromentin et al. 2014a). This high value, coupled with poor governance, led to three decades of high fishing pressure and ultimately to overexploitation. By 2011, ABFT was considered endangered by the IUCN (Collette et al. 2011). Following the implementation of a strict management plan in the late 1990’s, signs of population rebuilding have been documented (ICCAT 2021), but uncertainties around ABFT biology suggest that an overly simplistic management paradigm could compromise the long-term conservation of the species (Fromentin et al. 2014a, Brophy et al. 2020). ABFT has been managed as two separate units since 1981: the Western and Eastern stocks, which are separated by the 45°W meridian and are assumed to originate from the two spawning areas located in the Gulf of Mexico and the Mediterranean Sea respectively (ICCAT 2019). Several studies on the population structure and stock dynamics support two reproductively isolated spawning components (Gulf of Mexico and the Mediterranean Sea): electronic tagging studies (Block et al. 2005) have found no individual visiting both spawning areas, and otolith chemical signatures (Rooker et al. 2014) and genetic data (Rodríguez-Ezpeleta et al. 2019) support natal homing. Nevertheless, numerous studies also detected evidence of regular trans-Atlantic movements across the 45°W meridian boundary line and of mixed foraging grounds along the North Atlantic (Block et al. 2005, Rooker et al. 2014, Arregui et al. 2018, Rodríguez-Ezpeleta et al. 2019). In response to these findings, the International Commission for the Conservation of Atlantic Tunas (ICCAT) recently adopted a management procedure for ABFT that accounts for mixing between the two stocks (ICCAT 2023). Given recent advancements in stock of origin assignment and increased samples from the mixing areas, it is important to determine if the modeled dynamics are consistent with the new data. Specifically, when applying individual origin assignment based on subsets of informative genetic markers of ABFT captured in the North Atlantic Ocean (Rodríguez-Ezpeleta et al. 2019, Puncher et al. 2022), it was observed that 10-25% of individuals could not be clearly assigned to either spawning ground. Moreover, a combined analysis of genetic and otolith microchemistry data resulted in contrasting or unresolved origin assignments (Brophy et al. 2020).
Amidst uncertainty surrounding ABFT stock dynamics, the recent discovery of ABFT larvae in the Slope Sea (Richardson et al. 2016a) adds another layer of complexity to our knowledge of the reproductive ecology of the species. Subsequent oceanographic studies (Rypina et al. 2019) and larval collections (Hernández et al. 2022) provide additional evidence of spawning activity in this area. Tagging information further revealed that mature size fish occurred in the Slope Sea in spring and summer coinciding with the spawning season estimated for the found larvae (Galuardi et al. 2010), supporting the hypothesis of spawning strategy in the western Atlantic. The implications of Slope Sea spawning generated debate and controversy (Richardson et al. 2016b, Safina 2016, Walter et al. 2016), with one of the key unknowns being the connectivity between the Slope Sea and the other two spawning grounds. In addition, some studies found evidence of migratory changes in ABFT, including the return to (Horton et al. 2020, Nøttestad et al. 2020, Aarestrup et al. 2022) and even expansion (Jansen et al. 2021) of its geographic range. These changes coincided with a strong recovery of the Mediterranean Sea spawning biomass during the last two decades and the increased presence of eastern origin fish in the western Atlantic (Aalto et al. 2021).
To disentangle the population structure and connectivity of ABFT, we genotyped and analyzed thousands of genome-wide single nucleotide polymorphism (SNPs) from a total of five hundred ABFT larvae, young of the year (YoY) and adults from the two well-known spawning grounds (Gulf of Mexico and Mediterranean Sea) as well as the recently discovered Slope Sea spawning ground. We studied individual genomic diversity, tested for admixture between spawning grounds and inferred the demographic history of ABFT for the first time. We screened for adaptive genomic variation, incorporating samples from other Thunnusspecies to evaluate the impact of gene flow between species as an additional contribution to adaptive genomic diversity. Finally, we integrated information obtained from neutral, potentially adaptive and introgressed genetic markers to reconstruct the connectivity patterns of the ABFT across its entire distribution.