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.