Inter-specific gene introgression from albacore to Atlantic
bluefin tuna
We detected for the first-time signatures of introgression from albacore
tuna in the nuclear genome of the ABFT, which contradicts a previous
report (Ciezarek et al. 2018). The most
probable inter-lineage gene flow event estimated by the TreeMix analysis
happened between the albacore and the ABFT Mediterranean population. The
presence of mitochondrial introgression has also been reported in PBFT
(Chow and Kishino 1995); however,
although we included very few PBFT samples, we did not find any sign of
nuclear introgression in this species. Considering that ABFT and PBFT
evolved from a recent common ancestor
(Díaz-Arce et al. 2016) and that they
show very little genetic divergence, our results suggests that
introgression between albacore tuna and ABFT happened after the split
between the ABFT and PBFT lineages. Thus, to explain the presence of
albacore-like mitochondrial genomes in PBFT we hypothesize either
parallel introgression events between albacore tuna and both ABFT and
PBFT, or that mitochondrial introgressed genomes present in PBFT have
been introgressed through genetic exchanges with the ABFT. Likewise,
among ABFT individuals, the signal of introgression from albacore is
stronger in the Mediterranean and the Slope Sea and nearly absent in the
Gulf of Mexico. Thus, we conclude that introgression from albacore most
likely occurred in the Mediterranean ABFT population, where spawning
areas for ABFT and albacore overlap
(Alemany et al. 2010), and was
subsequently transmitted to the Slope Sea. Besides, the nearly complete
absence of both nuclear and mitochondrial introgression in Gulf of
Mexico individuals suggests that introgression happened after the split
between MED-like and GOM-like ancestral lineages which is consistent
with the inferred scenario of historically restricted gene flow between
east Atlantic and the Gulf of Mexico spawning components. Overall, the
east-west gradient of introgressed albacore alleles confirms the
inferred connectivity patterns presented in this study.
We identified a particular genomic region with characteristics typical
of a chromosomal inversion, such as high linkage disequilibrium and
increased heterozygosity values in samples occupying intermediate
positions in a local PCA (Barth et al.
2019, Puncher et al. 2019,
Jiménez-Mena et al. 2020). Our analysis
supports that, as reported for other species
(Jay et al. 2018), the origin of this
inversion was introduced into the ABFT genome as the result of a past
introgression event from albacore tuna. This region aggregates a high
number of outlier genetic markers. However, high linkage-disequilibrium
could bias towards the detection of false positives within this region
due to the synergic signal of dozens of variants. We could not associate
the presence of this introgression nor chromosomal inversion with
ecological or environmental factors; yet, introgression represents an
important source of genetic adaptive variation playing an important role
favoring speciation through processes such as introgression of favored
alleles (Arnold and Martin 2009,
Hedrick 2013,
Clarkson et al. 2014) or reproductive
isolation (Abbott et al. 2013,
Duranton et al. 2020). Moreover, the
literature abounds with examples showing that chromosomal inversions are
associated with local adaptation in the presence of gene flow
(Berg et al. 2016,
Barth et al. 2017a,
Wellenreuther and Bernatchez 2018,
Huang et al. 2020,
Le Moan et al. 2020,
Mérot et al. 2021,
Thorstensen et al. 2022). Given that
allele frequency differences between the Mediterranean and the Gulf of
Mexico components are stronger in the candidate chromosomal inversion
than the mean genome-wide differentiation, ascertaining its role in the
ABFT adaptation could be of great relevance to understand the species
resilience to changes in environmental conditions
(Muhling et al. 2011,
Erauskin-Extramiana et al. 2019).