Ada Natoli

Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus)

Bottlenose dolphins (Tursiops truncatus) are widely distributed and a high degree of morphometric and genetic differentiation has been found among both allopatric and parapatric populations. We analysed 145 samples along a contiguous distributional range from the Black Sea to the eastern North Atlantic for mitochondrial and nuclear genetic diversity, and found population structure with boundaries that coincided with transitions between habitat regions. These regions can be characterized by ocean floor topography, and oceanographic features such as surface salinity, productivity and temperature. At the extremes of this range there was evidence for the directional emigration of females. Bi-parentally inherited markers did not show this directional bias in migration, suggesting a different dispersal strategy for males and females at range margins. However, comparative assessment based on mitochondrial DNA and nuclear markers indicated that neither sex showed a strong bias for greater dispersal on average. These data imply a mechanism for the evolutionary structuring of populations based on local habitat dependence for both males and females.

Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses

Bottlenose dolphins (Tursiops truncatus) have a world‐wide distribution, and show morphotypic variation among regions. Distinctions between coastal and pelagic populations have been documented; however, regional patterns of differentiation had not been previously investigated in a wider geographic context. We analysed up to nine different populations from seven different areas of the world by mitochondrial DNA and microsatellite DNA markers, and found differentiation among all putative regional populations. Both mtDNA and microsatellite DNA data show significant differentiation, suggesting restricted gene flow for both males and females. Dolphins in coastal habitat showed less variability and were in most cases differentiated from a pelagic lineage, which could suggest local founder events in some cases. Two coastal populations recently classified as belonging to a new species, T. aduncus, were each highly differentiated from populations of the truncatus morphotype, and from each other, suggesting a possible third species represented by the South African aduncus type.

Low worldwide genetic diversity in the killer whale (Orcinus orca): implications for demographic history.

A low level of genetic variation in mammalian populations where the census population size is relatively large has been attributed to various factors, such as a naturally small effective population size, historical bottlenecks and social behaviour. The killer whale (Orcinus orca) is an abundant, highly social species with reduced genetic variation. We find no consistent geographical pattern of global diversity and no mtDNA variation within some regional populations. The regional lack of variation is likely to be due to the strict matrilineal expansion of local populations. The worldwide pattern and paucity of diversity may indicate a historical bottleneck as an additional factor.

Phylogeography and alpha taxonomy of the common dolphin (Delphinus sp.)

The resolution of taxonomic classifications for delphinid cetaceans has been problematic, especially for species in the genera Delphinus, Tursiops and Stenella. The frequent lack of correspondence between morphological and genetic differentiation in these species raises questions about the mechanisms responsible for their evolution. In this study we focus on the genus Delphinus, and use molecular markers to address questions about speciation and the evolution of population structure. Delphinus species have a worldwide distribution and show a high degree of morphological variation. Two distinct morphotypes, long‐beaked and short‐beaked, have been considered different species named D. capensis and D. delphis, respectively. However, genetic differentiation between these two forms has only been demonstrated in the Pacific. We analysed samples from eight different geographical regions, including two morphologically defined long‐beaked form populations, and compared these with the eastern North Pacific populations. We found high differentiation among the populations described as long‐beaked instead of the expected monophyly, suggesting that these populations may have evolved from independent events converging on the same morphotype. We observed low genetic differentiation among the short‐beaked populations across a large geographical scale. We interpret these phylogeographical patterns in the context of life history and population structure in related species.

Recent Diversification of a Marine Genus (Tursiops spp.) Tracks Habitat Preference and Environmental Change

Understanding the evolution of diversity and the resulting systematics in marine systems is confounded by the lack of clear boundaries in oceanic habitats, especially for highly mobile species like marine mammals. Dolphin populations and sibling species often show differentiation between coastal and offshore habitats, similar to the pelagic/littoral or benthic differentiation seen for some species of fish. Here we test the hypothesis that lineages within the polytypic genus Tursiops track past changes in the environment reflecting ecological drivers of evolution facilitated by habitat release. We used a known recent time point for calibration (the opening of the Bosphorus) and whole mitochondrial genome (mitogenome) sequences for high phylogenetic resolution. The pattern of lineage formation suggested an origin in Australasia and several early divisions involving forms currently inhabiting coastal habitats. Radiation in pelagic environments was relatively recent, and was likely followed by a return to coastal habitat in some regions. The timing of some nodes defining different ecotypes within the genus clustered near the two most recent interglacial transitions. A signal for an increase in diversification was also seen for dates after the last glacial maximum. Together these data suggest the tracking of habitat preference during geographic expansions, followed by transition points reflecting habitat shifts, which were likely associated with periods of environmental change.

Atypical panmixia in a European dolphin species (Delphinus delphis): implications for the evolution of diversity across oceanic boundaries

Despite the scarcity of geographical barriers in the ocean environment, delphinid cetaceans often exhibit marked patterns of population structure on a regional scale. The European coastline is a prime example, with species exhibiting population structure across well‐defined environmental boundaries. Here we undertake a comprehensive population genetic study on the European common dolphin (Delphinus delphis, based on 492 samples and 15 loci) and establish that this species shows exceptional panmixia across most of the study range. We found differentiation only between the eastern and western Mediterranean, consistent with earlier studies, and here use approximate Bayesian computations to explore different scenarios to explain the observed pattern. Our results suggest that a recent population bottleneck likely contributed significantly to the differentiation of the Eastern Mediterranean population (in Greek waters). This interpretation is consistent with independent census data that suggest a sharp population decline in the recent past. The implication is that an unperturbed population may currently show panmixia across the full study range. This exception to the more typical pattern of population structure seen for other regional dolphin species (and for common dolphin populations elsewhere in the world) suggests particular ecological or life‐history traits distinct to this species in European waters.

Balancing and Directional Selection at Exon-2 of the MHC DQB1 Locus among Populations of Odontocete Cetaceans

The diversity of exon-2 (peptide-binding region) of the DQB1 locus (Class II, major histocompatibility complex, MHC) was investigated on an extended sample of populations of three focal cetacean species (two sibling delphinid species and another in the same family). We tested the hypothesis that dolphin populations with a worldwide distribution across different habitats and geographic regions will be under differential selective pressure by comparing DQB1 variation with variation at neutral markers and by investigating putative functional residues within the exon-2 sequence at the population level. Variation at the DQB1 locus was not correlated to neutral differentiation (assessed by comparison with microsatellite DNA markers), and overall F(ST) values were significantly lower for the MHC locus, consistent with expectations for balancing selection. Measures of heterozygosity and d(n)/d(s) ratios were also consistent with balancing selection. However, outliers in the F(ST) comparisons and the analysis of putative functional residues suggested incidences of directional selection in local populations.

Patterns of Population Structure for Inshore Bottlenose Dolphins along the Eastern United States

Globally distributed, the bottlenose dolphin (Tursiops truncatus) is found in a range of offshore and coastal habitats. Using 15 microsatellite loci and mtDNA control region sequences, we investigated patterns of genetic differentiation among putative populations along the eastern US shoreline (the Indian River Lagoon, Florida, and Charleston Harbor, South Carolina) (microsatellite analyses: n = 125, mtDNA analyses: n = 132). We further utilized the mtDNA to compare these populations with those from the Northwest Atlantic, Gulf of Mexico, and Caribbean. Results showed strong differentiation among inshore, alongshore, and offshore habitats (ФST = 0.744). In addition, Bayesian clustering analyses revealed the presence of 2 genetic clusters (populations) within the 250 km Indian River Lagoon. Habitat heterogeneity is likely an important force diversifying bottlenose dolphin populations through its influence on social behavior and foraging strategy. We propose that the spatial pattern of genetic variation within the lagoon reflects both its steep longitudinal transition of climate and also its historical discontinuity and recent connection as part of Intracoastal Waterway development. These findings have important management implications as they emphasize the role of habitat and the consequence of its modification in shaping bottlenose dolphin population structure and highlight the possibility of multiple management units existing in discrete inshore habitats along the entire eastern US shoreline.

The Gulf of Ambracia's Common Bottlenose Dolphins, Tursiops truncatus: A Highly Dense and yet Threatened Population

The common bottlenose dolphin (Tursiops truncatus) is the only cetacean present in the semiclosed waters of the Gulf of Ambracia, Western Greece. This increasingly degraded coastal ecosystem hosts one of the highest observed densities in the Mediterranean Sea for this species. Photo-identification data and tissue samples collected through skin-swabbing and remote biopsy sampling techniques during boat-based surveys conducted between 2006 and 2015 in the Gulf, were used to examine bottlenose dolphin abundance, population trends, site fidelity, genetic differentiation and toxicological status. Bottlenose dolphins showed high levels of year-round site fidelity throughout the 10-year study period. Dolphin population estimates mostly fell between 130 and 170 with CVs averaging about 10%; a trend in population size over the 10 years was a decline of 1.6% per year (but this was not significant). Genetic differentiation between the bottlenose dolphins of the Gulf and their conspecifics from neighbouring populations was detected, and low genetic diversity was found among individuals sampled. In addition, pesticides where identified as factors posing a real toxicological problem for local bottlenose dolphins. Therefore, in the Gulf of Ambracia, high dolphin density does not seem to be indicative of favourable conservation status or pristine habitat.

Evolution of Functional Genes in Cetaceans Driven by Natural Selection on a Phylogenetic and Population Level

Cetaceans represent an evolutionary lineage marked by drastic morphological and physiological changes during their adaptation to an exclusively marine existence. In addition, several cetacean species exhibit geographical ranges that encompass different marine environments, with genetic breaks being sometimes consistent with environmental breaks. As such, genes that underwent adaptation during the land-sea transition can also be potential candidates for adaptation to different oceanic environments. In this study, we analysed 3 milk protein genes (β-casein, κ-casein, and α-lactalbumin) and 2 immunity related genes (MHCDQβ1 and γ-fibrinogen) for selection based on available phylogenetic datasets of both mammals and cetaceans, and used the results from this analysis to assess adaptation to different environments on a population level in the European common dolphin (Delphinus delphis). We found that evidence for positive selection could be detected in all genes in the phylogenetic analyses, with β-casein showing a further increase in selective pressure in the cetacean lineage. At the population level, both the immune system locus DQβ1 and β-casein genes showed patterns of variation consistent with divergent selection, and in each case the same populations showed differentiation. One of these populations was also differentiated at neutral markers, while the other was not. We discuss possible inference, and the potential for the further development of these ideas using genomic technologies.