Observed genetic differentiation between Atlantic bluefin tuna
spawning components cannot be attributed to local adaptation acting on
few loci of large effect
To better understand the evolutionary processes behind genetic
differentiation in ABFT, we separately studied genetic diversity at
neutral (i.e. those that are mostly influenced by genetic drift and
migration) and outlier SNPs markers (i.e. those that are potentially
under selection or in tight linkage with selected loci). Removing the
123 identified outlier markers did not change the overall population
structure pattern nor differentiation values (Figure S9), suggesting
that observed genetic differentiation cannot be explained by local
adaptation only. On the other hand, analyses based on the 123 markers
identified as potentially under selection provided higher genetic
differentiation values among spawning grounds (Figure S9) but revealed
three groups of samples that do not correspond to the overall population
structure (Figure 3A and S10) and that are neither related to laboratory
nor phenotypic sex effects (Figure S11). The 20% of the SNP markers
that contribute the most to this grouping are located within the same
region of the genome (mapping on two scaffolds spanning 2.63 Mb region
of the PBFT reference genome) (Table S7) and show strong pairwise
linkage disequilibrium (LD) across the whole region (meaning that
variant versions of SNP pairs are non-randomly associated and the same
combination is often found among individuals haplotypes) (Figure 3B).
The SNPs located within this high-LD region support a three-grouping
pattern (Figure S12), with the intermediate group of individuals in the
PCA presenting increased heterozygosity values (Figure 3C). This
suggests the existence of two main haplotypes (unique allelic
combinations across multiple SNPs) in this region combined into three
possible genotypes (e.g. AA, AB, BB), which shows characteristics
typical of a chromosomal inversion. These two haplotypes, presumably the
inverted and collinear versions, are present at different frequencies
among spawning grounds, the rarest found to be homozygous only in the
Mediterranean Sea, where it is more frequent, and the alternative being
more abundant in the Gulf of Mexico and Slope Sea (Figure 3D). A PCA
based on genetic markers from this genomic region including otherThunnus species (Figure 4A) showed that homozygous individuals
for the most abundant haplotype group associated with the PBFT, whereas
those homozygous for the rarest variant were close to albacore. By
contrast, the PCA based on the genome-wide SNP dataset showed the
expected grouping pattern reflecting species membership, where PBFT and
ABFT cluster together and were separated from albacore and Southern
bluefin tunas (Figure S13). Test for deviation from a strict bifurcating
evolutionary history (ABBA/BABA) showed a much more pronounced signal of
introgression from albacore into the Mediterranean and Slope Sea
spawning ground samples in the high-LD region (Figure 4B) than when
considering the overall genome (Figure 2B). Yet, this pattern remained
when removing all SNPs from the high-LD region (Figure S14), indicating
that the signal of introgression is present genome-wide.
These results suggest that the genetic differentiation observed between
ABFT from different spawning grounds is maintained despite gene flow
between the Mediterranean Sea and the Slope Sea and cannot be explained
by local adaptation acting on a few loci of large effect. Additionally,
a large genomic region of albacore ancestry, introgressed into the ABFT
genome in the Mediterranean Sea, has retained high LD while expanding
towards the western Atlantic, following the previously detected
genome-wide signal of albacore ancestry. Altogether, our results point
towards a situation where the two ancestral genetic components of ABFT
(Western Atlantic and Mediterranean) have initially diverged in
isolation, independently experiencing genetic drift combined with
introgression of genetic material from albacore in the Mediterranean
Sea. More recently, homogenization between western Atlantic and
Mediterranean components could have been initiated by the
intensification of gene flow, without completely eroding existing
genetic differentiation.