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).