Genomic Divergence and the Evolution of Ecotypes in Bottlenose Dolphins (Genus Tursiops).

Climatic changes have caused major environmental restructuring throughout the world's oceans. Marine organisms have responded to novel conditions through various biological systems, including genomic adaptation. Growing accessibility of next-generation DNA sequencing methods to study nonmodel species has recently allowed genomic changes underlying environmental adaptations to be investigated. This study used double-digest restriction-site associated DNA (ddRAD) sequence data to investigate the genomic basis of ecotype formation across currently recognized species and subspecies of bottlenose dolphins (genus Tursiops) in the Southern Hemisphere. Subspecies-level genomic divergence was confirmed between the offshore common bottlenose dolphin (T. truncatus truncatus) and the inshore Lahille's bottlenose dolphin (T. t. gephyreus) from the southwestern Atlantic Ocean (SWAO). Similarly, subspecies-level divergence is suggested between inshore (eastern Australia) Indo-Pacific bottlenose dolphin (T. aduncus) and the proposed Burrunan dolphin (T. australis) from southern Australia. Inshore bottlenose dolphin lineages generally had lower genomic diversity than offshore lineages, a pattern particularly evident for T. t. gephyreus, which showed exceptionally low diversity. Genomic regions associated with cardiovascular, musculoskeletal, and energy production systems appear to have undergone repeated adaptive evolution in inshore lineages across the Southern Hemisphere. We hypothesize that comparable selective pressures in the inshore environment drove similar adaptive responses in each lineage, supporting parallel evolution of inshore bottlenose dolphins. With climate change altering marine ecosystems worldwide, it is crucial to gain an understanding of the adaptive capacity of local species and populations. Our study provides insights into key adaptive pathways that may be important for the long-term survival of cetaceans and other organisms in a changing marine environment.

Directional selection on body size but no apparent survival cost to being large in wild New Zealand giraffe weevils.

When an individual's reproductive success relies on winning fights to secure mating opportunities, bearing larger weapons is advantageous. However, sexual selection can be extremely complex, and over an animal's life the opportunity to mate is influenced by numerous factors. We studied a wild population of giraffe weevils (Lasiorhynchus barbicornis) that exhibit enormous intra and intersexual size variation. Males bear an elongated rostrum used as a weapon in fights for mating opportunities. However, small males also employ sneaking behavior as an alternative reproductive tactic. We investigated sexual selection on size by tracking individual males and females daily over two 30-day periods to measure long-term mating success. We also assessed how survival and recapture probabilities vary with sex and size to determine whether there might be a survival cost associated with size. We found evidence for directional selection on size through higher mating success, but no apparent survival trade-off. Instead, larger individuals mate more often and have a higher survival probability, suggesting an accumulation of benefits to bigger individuals. Furthermore, we found evidence of size assortative mating where males appear to selectively mate with bigger females. Larger and more competitive males secure matings with larger females more frequently than smaller males, which may further increase their fitness.

Correction: Challenges of implementing Mark-recapture studies on poorly marked gregarious delphinids.

[This corrects the article DOI: 10.1371/journal.pone.0198167.].

Challenges of implementing Mark-recapture studies on poorly marked gregarious delphinids.

Population parameters of poorly marked gregarious species are difficult to estimate. This is the case for common dolphins (Delphinus sp.), a genus known for its lack of distinctive marks resulting in a low mark ratio. Furthermore, the widespread nature of common dolphins results in low recaptures. We developed reliable photo-identification protocols to ensure accurate identification of individuals in the Hauraki Gulf, New Zealand. These protocols combined the use of nicks and notches and pigmentation patterns for identification and included the development of a distinctiveness threshold. The data were further stratified by the level of distinctiveness of each individual (as distinctive or highly-distinctive). Photo-identification surveys were conducted from January 2010 to December 2013. Mark-recapture techniques were implemented through a POPAN super-population approach to estimate seasonal apparent survival, capture probability and abundance of dolphins. A total of 2,083 unique adult common dolphins were identified, 51.3% were classified as D1 (highly distinctive; n = 1,069) and 48.7% as D2 (distinctive; n = 1,014). Of all individuals identified, 34.3% (n = 704) were re-sighted over subsequent years. The proportion of marked dolphins (when compared to unmarked dolphins) was 26.3% for D1 and 46.4% for D1 & D2, respectively. Apparent survival was estimated at 0.767 (CI = 0.694-0.827) for D1 animals, and 0.796 (CI = 0.729-0.850) for D1 & D2 combined. For D1 only, seasonal abundance varied from 732 (CI = 460-1,177) in autumn 2010 to 5,304 (CI = 4,745-5,930) in spring 2013. While the inclusion of D2 individuals may offer a more precise estimate of total abundance, the inability to determine additional sources of bias (for example, arising from under or overestimated mark ratios) meant that estimates for D1 individuals were deemed the least biased for this population. The photo-identification protocol, stratification of the data and steps taken to eliminate potential model violations provided a useful and novel approach to estimate population parameters for common dolphins. These approaches could be implemented for other large gregarious populations (≥500 individuals) of animals with poor natural markings.

High genetic structure and low mitochondrial diversity in bottlenose dolphins of the Archipelago of Bocas del Toro, Panama: A population at risk?

The current conservation status of the bottlenose dolphin (Tursiops truncatus) under the IUCN is 'least concern'. However, in the Caribbean, small and localized populations of the 'inshore form' may be at higher risk of extinction than the 'worldwide distributed form' due to a combination of factors including small population size, high site fidelity, genetic isolation, and range overlap with human activities. Here, we study the population genetic structure of bottlenose dolphins from the Archipelago of Bocas del Toro in Panama. This is a small population characterized by high site fidelity and is currently heavily-impacted by the local dolphin-watching industry. We collected skin tissue samples from 25 dolphins to study the genetic diversity and structure of this population. We amplified a portion of the mitochondrial Control Region (mtDNA-CR) and nine microsatellite loci. The mtDNA-CR analyses revealed that dolphins in Bocas del Toro belong to the 'inshore form', grouped with the Bahamas-Colombia-Cuba-Mexico population unit. They also possess a unique haplotype new for the Caribbean. The microsatellite data indicated that the Bocas del Toro dolphin population is highly structured, likely due to restricted movement patterns. Previous abundance estimates obtained with mark-recapture methods reported a small population of 80 dolphins (95% CI = 72-87), which is similar to the contemporary effective population size estimated in this study (Ne = 73 individuals; CI = 18.0 - ∞; 0.05). The combination of small population size, high degree of genetic isolation, and intense daily interactions with dolphin-watching boats puts the Bocas del Toro dolphin to at high risk of extinction. Despite national guidelines to regulate the dolphin-watching industry in Bocas del Toro and ongoing educational programs for tour operators, only in 2012 seven animals have died due to boat collisions. Our results suggest that the conservation status of bottlenose dolphins in Bocas del Toro should be elevated to 'endangered' at the national level, as a precautionary measure while population and viability estimates are conducted.

A worldwide perspective on the population structure and genetic diversity of bottlenose dolphins (Tursiops truncatus) in New Zealand.

Bottlenose dolphins (Tursiops truncatus) occupy a wide range of coastal and pelagic habitats throughout tropical and temperate waters worldwide. In some regions, "inshore" and "offshore" forms or ecotypes differ genetically and morphologically, despite no obvious boundaries to interchange. Around New Zealand, bottlenose dolphins inhabit 3 coastal regions: Northland, Marlborough Sounds, and Fiordland. Previous demographic studies showed no interchange of individuals among these populations. Here, we describe the genetic structure and diversity of these populations using skin samples collected with a remote biopsy dart. Analysis of the molecular variance from mitochondrial DNA (mtDNA) control region sequences (n = 193) showed considerable differentiation among populations (F(ST) = 0.17, Phi(ST) = 0.21, P < 0.001) suggesting little or no female gene flow or interchange. All 3 populations showed higher mtDNA diversity than expected given their small population sizes and isolation. To explain the source of this variation, 22 control region haplotypes from New Zealand were compared with 108 haplotypes worldwide representing 586 individuals from 19 populations and including both inshore and offshore ecotypes as described in the Western North Atlantic. All haplotypes found in the Pacific, regardless of population habitat use (i.e., coastal or pelagic), are more divergent from populations described as inshore ecotype in the Western North Atlantic than from populations described as offshore ecotype. Analysis of gene flow indicated long-distance dispersal among coastal and pelagic populations worldwide (except for those haplotypes described as inshore ecotype in the Western North Atlantic), suggesting that these populations are interconnected on an evolutionary timescale. This finding suggests that habitat specialization has occurred independently in different ocean basins, perhaps with Tursiops aduncus filling the ecological niche of the inshore ecotype in some coastal regions of the Indian and Western Pacific Oceans.