Genomics of Population Differentiation in Humpback Dolphins, Sousa spp. in the Indo-Pacific Ocean.

Speciation is a fundamental process in evolution and crucial to the formation of biodiversity. It is a continuous and complex process, which can involve multiple interacting barriers leading to heterogeneous genomic landscapes with various peaks of divergence among populations. In this study, we used a population genomics approach to gain insights on the speciation process and to understand the population structure within the genus Sousa across its distribution in the Indo-Pacific region. We found 5 distinct clusters, corresponding to S. plumbea along the eastern African coast and the Arabian Sea, the Bangladesh population, S. chinensis off Thailand and S. sahulensis off Australian waters. We suggest that the high level of differentiation found, even across geographically close areas, is likely determined by different oceanographic features such as sea surface temperature and primary productivity.

Killer whale genomes reveal a complex history of recurrent admixture and vicariance.

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to four-fold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

The world's most isolated and distinct whale population? Humpback whales of the Arabian Sea.

A clear understanding of population structure is essential for assessing conservation status and implementing management strategies. A small, non-migratory population of humpback whales in the Arabian Sea is classified as "Endangered" on the IUCN Red List of Threatened Species, an assessment constrained by a lack of data, including limited understanding of its relationship to other populations. We analysed 11 microsatellite markers and mitochondrial DNA sequences extracted from 67 Arabian Sea humpback whale tissue samples and compared them to equivalent datasets from the Southern Hemisphere and North Pacific. Results show that the Arabian Sea population is highly distinct; estimates of gene flow and divergence times suggest a Southern Indian Ocean origin but indicate that it has been isolated for approximately 70,000 years, remarkable for a species that is typically highly migratory. Genetic diversity values are significantly lower than those obtained for Southern Hemisphere populations and signatures of ancient and recent genetic bottlenecks were identified. Our findings suggest this is the world's most isolated humpback whale population, which, when combined with low population abundance estimates and anthropogenic threats, raises concern for its survival. We recommend an amendment of the status of the population to "Critically Endangered" on the IUCN Red List.

Hybrid speciation in a marine mammal: the clymene dolphin (Stenella clymene).

Natural hybridization may result in the exchange of genetic material between divergent lineages and even the formation of new taxa. Many of the Neo-Darwinian architects argued that, particularly for animal clades, natural hybridization was maladaptive. Recent evidence, however, has falsified this hypothesis, instead indicating that this process may lead to increased biodiversity through the formation of new species. Although such cases of hybrid speciation have been described in plants, fish and insects, they are considered exceptionally rare in mammals. Here we present evidence for a marine mammal, Stenella clymene, arising through natural hybridization. We found phylogenetic discordance between mitochondrial and nuclear markers, which, coupled with a pattern of transgressive segregation seen in the morphometric variation of some characters, support a case of hybrid speciation. S. clymene is currently genetically differentiated from its putative parental species, Stenella coerueloalba and Stenella longisrostris, although low levels of introgressive hybridization may be occurring. Although non-reticulate forms of evolution, such as incomplete lineage sorting, could explain our genetic results, we consider that the genetic and morphological evidence taken together argue more convincingly towards a case of hybrid speciation. We anticipate that our study will bring attention to this important aspect of reticulate evolution in non-model mammal species. The study of speciation through hybridization is an excellent opportunity to understand the mechanisms leading to speciation in the context of gene flow.

Influences of past climatic changes on historical population structure and demography of a cosmopolitan marine predator, the common dolphin (genus Delphinus).

Climatic oscillations during the Pleistocene have greatly influenced the distribution and connectivity of many organisms, leading to extinctions but also generating biodiversity. While the effects of such changes have been extensively studied in the terrestrial environment, studies focusing on the marine realm are still scarce. Here we used sequence data from one mitochondrial and five nuclear loci to assess the potential influence of Pleistocene climatic changes on the phylogeography and demographic history of a cosmopolitan marine predator, the common dolphin (genus Delphinus). Population samples representing the three major morphotypes of Delphinus were obtained from 10 oceanic regions. Our results suggest that short-beaked common dolphins are likely to have originated in the eastern Indo-Pacific Ocean during the Pleistocene and expanded into the Atlantic Ocean through the Indian Ocean. On the other hand, long-beaked common dolphins appear to have evolved more recently and independently in several oceans. Our results also suggest that short-beaked common dolphins had recurrent demographic expansions concomitant with changes in sea surface temperature during the Pleistocene and its associated increases in resource availability, which differed between the North Atlantic and Pacific Ocean basins. By proposing how past environmental changes had an effect on the demography and speciation of a widely distributed marine mammal, we highlight the impacts that climate change may have on the distribution and abundance of marine predators and its ecological consequences for marine ecosystems.

Species tree of a recent radiation: the subfamily Delphininae (Cetacea, Mammalia).

Lineages undergoing rapid radiations provide exceptional opportunities for studying speciation and adaptation, but also represent a challenge for molecular systematics because retention of ancestral polymorphisms and the occurrence of hybridization can obscure relationships among lineages. Dolphins in the subfamily Delphininae are one such case. Non-monophyly, rapid speciation events, and discordance between morphological and molecular characters have made the inference of phylogenetic relationships within this subfamily very difficult. Here we approach this problem by applying multiple methods intended to estimate species trees using a multi-gene dataset for the Delphininae (Sousa, Sotalia, Stenella, Tursiops, Delphinus and Lagenodelphis). Incongruent gene trees obtained indicate that incomplete lineage sorting and possibly hybridization are confounding the inference of species history in this group. Nonetheless, using coalescent-based methods, we have been able to extract an underlying species-tree signal from divergent histories of independent genes. This is the first time a molecular study provides support for such relationships. This study further illustrates how methods of species-tree inference can be very sensitive both to the characteristics of the dataset and the evolutionary processes affecting the evolution of the group under study.

Seascape genetics of a globally distributed, highly mobile marine mammal: the short-beaked common dolphin (genus Delphinus).

Identifying which factors shape the distribution of intraspecific genetic diversity is central in evolutionary and conservation biology. In the marine realm, the absence of obvious barriers to dispersal can make this task more difficult. Nevertheless, recent studies have provided valuable insights into which factors may be shaping genetic structure in the world's oceans. These studies were, however, generally conducted on marine organisms with larval dispersal. Here, using a seascape genetics approach, we show that marine productivity and sea surface temperature are correlated with genetic structure in a highly mobile, widely distributed marine mammal species, the short-beaked common dolphin. Isolation by distance also appears to influence population divergence over larger geographical scales (i.e. across different ocean basins). We suggest that the relationship between environmental variables and population structure may be caused by prey behaviour, which is believed to determine common dolphins' movement patterns and preferred associations with certain oceanographic conditions. Our study highlights the role of oceanography in shaping genetic structure of a highly mobile and widely distributed top marine predator. Thus, seascape genetic studies can potentially track the biological effects of ongoing climate-change at oceanographic interfaces and also inform marine reserve design in relation to the distribution and genetic connectivity of charismatic and ecologically important megafauna.

Multi-locus species tree of the chub genus Squalius (Leuciscinae: Cyprinidae) from western Iberia: new insights into its evolutionary history.

The phylogenetic relationships of the genus Squalius are believed to be well established based on the mitochondrial cytochrome b gene. Here, we inferred the phylogenetic relationships of all species inhabiting most of the western Iberia river systems using a nuclear multi-locus approach and different species tree methods: concatenation and coalescent-based methods (BEST and minimize-deep-coalescence). The dataset comprised sequences of seven coding and three non-coding regions belonging to seven nuclear genes, which were chosen to cover multiple biological functions: amh, bmp4, ef1a, egr2, irbp, rh and rpl8. We provide evidence for a conflicting topology between the nuDNA species tree and the widely reported mtDNA gene tree. S. pyrenaicus is rendered paraphyletic in all nuDNA species trees, with populations of the Tagus/Colares clustering with S. carolitertii, while populations from the Guadiana, Sado and Almargem form a separate clade. Although a larger sampling size encompassing the full spectrum of Squalius populations in western Iberia is still needed to fully elucidate the phylogeography and species delimitation of this genus, our results suggest that the two S. pyrenaicus clades may represent different species.

Evolution of 2 reproductive proteins, ZP3 and PKDREJ, in cetaceans.

The rapid evolution of proteins involved in reproduction has been documented in several animal taxa. This is thought to be the result of forces involved in sexual selection and is expected to be particularly strong in promiscuous mating systems. In this study, a range of cetacean species were used to analyze the patterns of evolution in 2 reproductive proteins involved in fertilization: the zona pellucida 3 (ZP3), present in the egg coat, and PKDREJ, localized in the sperm head. We targeted exons 6 and 7 of ZP3 and a part of the REJ domain in PKDREJ for a total of 958 bp in 18 species. We found very low levels of amino acid sequence divergence in both proteins, a very weak signal of positive selection in ZP3 and no signal in PKDREJ. These results were consistent with previous reports of a slow rate of molecular evolution in cetaceans but unexpected due to the existence of promiscuous mating systems in these species. The results raise questions about the evolution of reproductive isolation and species recognition in whales and dolphins.

Cranial shape differentiation in three closely related delphinid cetacean species: insights into evolutionary history.

The present study investigates the pattern of differentiation of cranial shape in three closely related delphinid cetacean species of the complex Delphinus-Stenella-Tursiops: Delphinus delphis, Stenella coeruleoalba and Tursiops truncatus. Dorsal and ventral aspects of the cranium were analysed using landmark-based geometric morphometric methods. While there was no evidence of sexual dimorphism for shape or size, multivariate statistical analyses showed that there were interspecific differences in skull morphology. Skull shape differences between the three studied species were related with cranial width and differences in the length of the rostrum relative to the cranial portion of the skull. D. delphis and S. coeruleoalba showed high cranial shape similarity, which is indicative of their evolutionary proximity when compared with T. truncatus. Phenetic clusters based on cranial shape similarities were found to be concordant with the molecular phylogenetic clades obtained from mitochondrial DNA genes. Geometric morphometric methods can thus be an exceptionally useful tool for the study of differentiation of delphinid cetacean species and therefore provide some insights into their evolutionary history.