A genomic assessment of the marine-speciation paradox within the toothed whale superfamily Delphinoidea

Abstract

Understanding speciation is a central aspect in Biology. The formation of new species was once thought to be a simple bifurcation process. However, recent advances in genomic resources now provide the opportunity to investigate the role of post-divergence gene flow in the speciation process. The diversification of lineages in the presence of gene flow appears almost paradoxical. However, with enough time and in the presence of incomplete physical and/or ecological barriers to gene flow, speciation can and does occur. Speciation without complete isolation seems especially likely to occur in highly mobile, wide ranging marine species, such as cetaceans, which face limited geographic barriers. The toothed whale superfamily Delphinoidea represents a good example to further explore speciation in the presence of interspecific gene flow. Delphinoidea consists of three families (Delphinidae, Phocoenidae, and Monodontidae) and within all three families, contemporary interspecific hybrids have been reported. Here, we utilise publicly available genomes from nine species, representing all three families, to investigate signs of post-divergence gene flow across their genomes, and to address the speciation processes that led to the diversity seen today within Delphinoidea. We use a multifaceted approach including: (i) phylogenetics, (ii) the distribution of shared derived alleles, and (iii) demography-based. We find that the divergence and evolution of lineages in Delphinoidea did not follow a simple bifurcating pattern, but were much more complex. Our results indicate multiple, long-lasting ancestral gene flow events both within and among families, which continued for millions of years after initial divergence.

A Genetic Perspective on Cetacean Evolution

“…The authors found multiple ancestral gene flow events both within and among families, which continued for millions of years after initial divergence. These postdivergence gene flow events may also explain the presence of contemporaneous hybrids between several species (Westbury et al 2021). The documented cases of hybridization, together with the identified signals of introgression among species, provide unique examples of the complex evolutionary history of cetaceans.…”

“…Employing whole-genome sequences of nine species from three families (Delphinidae, Phocoenidae, and Monodontidae) of cetaceans, Westbury et al (2021) analyzed the presence of postdivergence gene flow across their genomes and addressed the speciation processes that led to the diversity observed today. The authors found multiple ancestral gene flow events both within and among families, which continued for millions of years after initial divergence.…”

“…Recent studies have shown how the use of different biomolecules can provide a more coherent approach to address certain evolutionary issues in cetaceans. These issues include analysis of adaptation using transcriptomics (Toren et al 2020), organ or system function employing proteomics (Kershaw et al 2018), and speciation and hybridization processes using comparative genomics (Westbury et al 2021). They also include the study of coevolution between cetaceans and microbial communities using metagenomics (Li et al 2019) and age estimation using epigenetics (Polanowski et al 2014), among others.…”

Genomics reveals the role of admixture in the evolution of structure among sperm whale populations within the Mediterranean Sea

“…In oceanic ecosystems, geographical barriers are often less relevant than oceanographic and other environmental factors in shaping the genetic structure of populations (e.g., Hoelzel, 1994; Palumbi, 2004; Van Cise et al, 2019; Westbury et al, 2022). Varying selection pressures, patterns of connectivity and genetic drift shape the diversity of species, potentially leading to greater geographical diversity in species with a wide latitudinal distribution range (Ralph & Coop, 2010).…”

“…In oceanic ecosystems, geographical barriers are often less relevant than oceanographic and other environmental factors in shaping the genetic structure of populations (e.g., Hoelzel, 1994;Palumbi, 2004;Van Cise et al, 2019;Westbury et al, 2022).…”