Selection on ancestral genetic variation fuels repeated ecotype formation in bottlenose dolphins

Abstract

Studying repeated adaptation can provide insights into the mechanisms allowing species to adapt to novel environments. Here, we investigate repeated evolution driven by habitat specialization in the common bottlenose dolphin. Parapatric pelagic and coastal ecotypes of common bottlenose dolphins have repeatedly formed across the oceans. Analyzing whole genomes of 57 individuals, we find that ecotype evolution involved a complex reticulated evolutionary history. We find parallel linked selection acted upon ancient alleles in geographically distant coastal populations, which were present as standing genetic variation in the pelagic populations. Candidate loci evolving under parallel linked selection were found in ancient tracts, suggesting recurrent bouts of selection through time. Therefore, despite the constraints of small effective population size and long generation time on the efficacy of selection, repeated adaptation in long-lived social species can be driven by a combination of ecological opportunities and selection acting on ancestral standing genetic variation.

Hybridization and a mixture of small and large-effect loci facilitate adaptive radiation

“…‘Albeli’ species included C. candidus, C. albellus , C. muelleri , and C. heglingus (for lakes Neuchâtel, Brienz, Lucerne, and Walen), and ‘Balchen’ species included C. palea, C. alpinus, C. litoralis , and C. duplex (for lakes Neuchâtel, Brienz, Lucerne, and Walen). To first confirm the independent evolution of each ‘Balchen’ and ‘Albeli’ species-pair within each of these four lakes, as indicated by the phylogeny, F4 statistics were calculated across a four-taxon tree (as used in 42 ), allowing us to estimate the degree of correlated allele frequencies between ‘Balchen’ and ‘Albeli’ individuals within and between lake-systems. First, loci were pruned based on linkage disequilibrium using the script ldPruning.sh (https://github.com/joanam/scripts/raw/master/ldPruning.sh), resulting in 1,315,105 SNPs.…”

“…To identify whether this parallel phenotypic differentiation was underpinned by parallel allele-frequency shifts we first investigated four sympatric pairs of 'Balchen' and 'Albeli' species from lakes Brienz, Lucerne, Walen, and Neuchâtel. We subsetted our full data set to include three 'Balchen' and three 'Albeli' individuals from each of these four lakes and first analysed F4 statistics to confirm that indeed each sympatric species-pair represents a single independently evolved species-pair (as in 42 ). Topologies placing sympatric 'Balchen' and 'Albeli' species as sister taxa in a four-taxon tree had consistently lower F4 statistics, indicative of a more accurate topology, than topologies where the species of the same ecomorph from different lakes were sister taxa (Supplementary Fig.…”

“…To identify the degree of genetic parallelism between 'Balchen' and 'Albeli' whitefish species from across the radiation, we subsetted 24 individuals representing three 'Balchen' species and three 'Albeli' species from four of the lakes we sampled: Lake Brienz, Lake Lucerne, Lake Walen and Brienz, Lucerne, and Walen). To first confirm the independent evolution of each 'Balchen' and 'Albeli' species-pair within each of these four lakes, as indicated by the phylogeny, F4 statistics were calculated across a four-taxon tree (as used in 42 ), allowing us to estimate the degree of correlated allele frequencies between 'Balchen' and 'Albeli' individuals within and between lake-systems. First, loci were pruned based on linkage disequilibrium using the script ldPruning.sh (https://github.com/joanam/scripts/raw/master/ldPruning.sh), resulting in 1,315,105 SNPs.…”

Chromosomal inversions can limit adaptation to new environments

“…Mounting empirical evidence suggests that standing genetic variation is the main source of genetic variation for the early phases of adaptation in nature (e.g., Renaut et al 2011; Jones et al 2012; Lescak et al 2015; Haenel et al 2019; Lai et al 2019; Chaturvedi et al 2021; Louis et al 2021; Owens et al 2021; Whiting et al 2021; see also Barrett & Schluter 2008; Messer & Petrov 2012; De Lafontaine et al 2018). Whether and how rapidly a population can adapt to a new ecological challenge therefore depends on how efficiently selection can reshape pre-existing alleles into new optimal combinations.…”

Seascape genomics of common dolphins (Delphinus delphis) reveals adaptive diversity linked to regional and local oceanography

“…In toothed whales (Odontoceti), most studies of adaptations using genomic markers have focused on a macroevolutionary perspective, while studies investigating ecological specialisation on a microevolutionary level have been documented only for a few species. This includes ecotype adaptations of killer whales (Orcinus orca [16]), spinner dolphins (Stenella longirostris [17]), finless porpoises (Neophocaena phocaenoides [18,19]), and bottlenose dolphins (Tursiops aduncus [20], and T. truncatus [21]). Despite these examples, population-level studies of microevolutionary processes remain highly under documented in Odontocetes, specifically in small cetaceans.…”