Evidence of presence of Mediterranean origin fish in the Gulf of
Mexico could suggest recent changes in Atlantic bluefin tuna
connectivity patterns
Overall, our results support a historical split between the western
Atlantic and Mediterranean spawning grounds followed by a subsequent
split between the Gulf of Mexico and Slope Sea and trans-Atlantic
unidirectional gene flow from the Mediterranean into western Atlantic
spawning grounds. While admixture in the Slope Sea is reflected in the
larval and juvenile individual genetic profiles, larvae captured in the
Gulf of Mexico were pure GOM-like. Previous work suggested weak input of
Mediterranean alleles in the larvae collected from the western Gulf of
Mexico in the year 2014 (Johnstone et al.
2021). However, we have not detected evidence of such genetic
connectivity in larval samples from the western and eastern sides of the
Gulf of Mexico collected before this date (from years 2007 to 2010)
despite using thousands of SNP genetic markers. Nevertheless, the number
of larvae collected in the Gulf of Mexico with individual genetic
profile available for this study remains limited (n=27) and the presence
of MED-like spawning adults suggests potential genetic connectivity
between the Mediterranean Sea and the Gulf of Mexico. Given that Slope
Sea individuals’ ancestry proportions cover the range of MED-like
individual genetic profiles, it would also be possible that these
MED-like individuals have their origin in the Slope Sea. The detection
of MED-like individuals in the Gulf of Mexico originating from the Slope
Sea is made likely due to its proximity.
Due to the heterogeneous profile of the Slope Sea, the observed
proportion of MED-like individuals in the Gulf of Mexico originated in
the Slope Sea could only be explained by a high number of Slope Sea
MED-like individuals entering the Gulf of Mexico, unless MED-like
individuals originated in the Slope Sea under a scenario of even higher
inflow from the eastern Atlantic. Otolith microchemistry analyses
revealed that genetically MED-like individuals captured in the Gulf of
Mexico showed an otolith isotopic composition of oxygen
(δ18O) intermediate between the Gulf of Mexico and the
Mediterranean spawning areas, suggesting that these were probably not
born in the Gulf of Mexico. Interestingly, these intermediate values are
consistent with the proposed signature range of a potential third
contingent, compatible with a Slope Sea or Mediterranean origin of
individuals showing early and/or more intense migratory behavior
(Brophy et al. 2020). These observations
allow for different possible origins of the MED-like individuals
captured in the Gulf of Mexico. Additional observations of the genetic
composition of adult ABFT spawning in the Slope Sea coupled with further
knowledge about the migratory behavior of Mediterranean ABFT would be
needed to assign the origin of these MED-like individuals more
accurately.
Regardless of the origin of the MED-like individuals in the Gulf of
Mexico, a few dozen migrants exchanged per generation is theoretically
sufficient to erase genetic differentiation between populations
(Waples 1998,
Lowe and Allendorf 2010,
Gagnaire et al. 2015). The low
FST values reported in this study are common among
marine fishes with large population sizes, high dispersal rates and
wide-ranging distributions (Hauser and
Carvalho 2008, da Fonseca et al. 2022,
Fuentes-Pardo et al. 2022). While genetic
differentiation of ABFT between the Mediterranean Sea and the Gulf of
Mexico could persist despite admixed individuals in the Slope Sea, the
number of migrants detected in the Gulf of Mexico is theoretically
expected to lead to genetic homogeneity between eastern and western born
ABFT and is thus not easily compatible with significant
FST values. Histological inspection confirmed the
presence of at least one MED-like female which had spawned less than 48
hours before capture in the Gulf of Mexico, suggesting that MED-like
individuals spawn in the Gulf of Mexico. One possible explanation for
the observed levels of genetic differentiation would be negative
selection against Mediterranean genes preventing successful gene flow.
Hence, we have explored different sources of genetic variation, which
could help to explain the maintenance of genetic differentiation between
highly demographically connected populations. More specifically, we have
explored the effect of locally adaptive alleles, which could maintain
genetic differentiation in the presence of gene flow
(Tigano and Friesen 2016) and
inter-specific introgression, which can trigger different evolutionary
processes, such as the input of adaptive alleles
(Huerta-Sánchez et al. 2014) or the
contribution to reproductive isolation
(Duranton et al. 2020). However, we did
not find evidence to confirm the maintenance of genetic differentiation
through either local adaptation or reproductive isolation. These would
lead to much higher levels of FST at loci involved in
incompatibilities and/or selection than the ones observed in this work.
Besides, genome-wide and homogeneously distributed genetic
differentiation between Mediterranean Sea and Gulf of Mexico reference
individuals at neutral alleles reflects that differentiation is not
primarily driven by introgression or adaptation, but by the effect of
historical long-term isolation between Mediterranean and Atlantic
populations, as indicated by their inferred demographic history.
Moreover, interbreeding in the Slope Sea implies genetic compatibility
between GOM-like and MED-like individuals, which makes the barrier to
gene flow hypothesis unlikely to explain the maintenance of genetic
differentiation. Another possibility is that selection undetected in
this study impedes incorporation of MED-like alleles in the Gulf of
Mexico. On one hand, widespread polygenic selection remains difficult to
reject based on outlier detection tests as the ones used here, as these
are underpowered to detect weakly selected loci, although genetic
differences are unlikely maintained by weak polygenic selection in the
presence of gene flow. On the other hand, the use of reduced
representation sequencing could lead to missed localized selective
sweeps. Analyses based on whole genome sequencing data would allow one
to detect adaptation signals missed in our study. Alternatively, we
propose that the currently observed ancestry patterns could be explained
by recent secondary contact following genetic divergence of both
ancestral populations after long-term isolation with reduced or no
migration, and that the high observed migration rates, in the absence of
barriers to gene flow and if sustained over time, could ultimately lead
to genetic homogenization and the consequently the loss of genetic
differentiation.