In a time of rapid climate change, a key question is how rapidly a species can adapt to new environmental conditions. Bottlenose dolphins have repeatedly adapted from pelagic to coastal habitat across the world 1–5, but we do not know how this parallel adaptation occurred and how fast this happened. To answer these questions can prove challenging in a species with long generation time such as bottlenose dolphins. To overcome this problem, we harnessed the power of paleogenomics and re-sequenced the genomes of four subfossils of bottlenose dolphins (8610-5626 years old), which lived around the time of the formation of new coastal habitat, after the ice sheets from the last glacial period retreated (Figure 1a-b). We compared those ancient genomes with genomes from contemporary pelagic and coastal bottlenose dolphins (Figure 1a) 3.

Figure 1. a) Sampling locations of the four ancient (black triangle) and 60 contemporary coastal (denoted with postscript ‘c’ and shown in shades of red) and pelagic (postscript ‘p’ and in shades of blue) bottlenose dolphins in the eastern North Atlantic (ENAc and ENAp), western North Atlantic (WNAc and WNAp) and eastern North Pacific (ENPc and ENPp). b) Mandible of a subfossil bottlenose dolphin (sample NMR10326) included in our study.

The subfossils of bottlenose dolphins were dredged from the bottom of the North Sea during fishing operations. They are now curated at the Natural History Museum of Rotterdam, and present an exceptional opportunity to work on the adaptation of bottlenose dolphins to coastal habitat. As these bones have been sitting at the bottom of the sea for thousands of years they have been subjected to  microbial and other animal activity since the organism’s death, and this was no exception for specimen SP1060 (Figure 2). This partial vertebra fragment has a rough crumbling dark surface, and is extremely porous and brittle from prolonged water damage. Endogenous DNA (i.e. DNA from a dolphin instead of  microbial or from any other species) preservation in the bone varies substantially, from 0.01% to about 5%. Luckily, this bone was one of several bones used to test a more controlled bleach decontamination approach 6 to increase the fraction of endogenous DNA prior to Illumina single stranded library preparation and sequencing. The bleach treated bone powder extract now contained around 44% DNA fragments that mapped to the dolphin reference genome. This allowed us to generate a high quality genome for the SP1060 individual, and reduced sequencing costs. We also generated whole genome sequencing data from three other subfossil specimens, using other methods aiming to get more DNA from the dolphins than microbes or other animals. We did not reach as high an endogenous content as for SP1060.

Figure 2. SP1060 before/after sampling for the bleach decontamination study 6, photo: Petra Korlević

We found that the subfossil specimens get genetically closer to coastal populations as the age of the specimens decreased. The oldest subfossil sample (NMR10326, 8,610 years old) clusters with the pelagic dolphins while the three others samples show more affinity with the North Atlantic coastal populations (Figure 3).

Figure 3. Principal component analysis of data from four ancient samples projected on the PCs of 60 contemporary samples (coastal in shades of red and pelagic in shade of blue) showing first and second PCs based on 624,969 SNPs. The proportion of genetic variance captured by each component is indicated in the axes.

We then focused on specimen SP1060, as it was high quality and had enough endogenous content to get invaluable insights on the adaptation history of bottlenose dolphins to coastal habitat. SP1060 is the youngest sample we worked with (5,626 years old). It was alive around, or shortly after, the putative time of colonisation of coastal waters by bottlenose dolphins in the North Sea and the emergence of coastal marine habitat in this region. SP1060 contained coastal-associated genotypes at sites previously inferred to be under parallel selection to coastal habitat in a recent study 3. This gives us insights on the speed of local adaptation and suggests that parallel adaptation occurred rapidly from genetic variation already present in the pelagic populations after the emergence of new coastal habitats. 

We also found introgression of coastal lineages into pelagic populations in the past, which may have reintroduced coastal-associated ancestry into pelagic populations. Natural selection could then have worked on this coastal-adapted ancestry to promote rapid local adaptation when new coastal habitat emerged. 

Using ancient samples, we could get insights on the pace and mechanisms of adaptation to coastal habitat, which would not have been possible with only contemporary genomes. Our study is one of the few that looks at adaptation in non-model and non domesticated species using paleogenomics. We hope it can be used as a roadmap for future studies of parallel evolution.

Post written by Petra Korlević and Marie Louis.

References

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2. Lowther-Thieleking, J. L., Archer, F. I., Lang, A. R. & Weller, D. W. Genetic differentiation among coastal and offshore common bottlenose dolphins, Tursiops truncatus, in the eastern North Pacific Ocean. Mar. Mamm. Sci. 31, 1–20 (2015).
3. Louis, M. et al. Selection on ancestral genetic variation fuels repeated ecotype formation in bottlenose dolphins. Sci Adv 7, eabg1245 (2021).
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