Ancient dolphin genomes reveal rapid repeated adaptation to coastal waters.

Parallel evolution provides strong evidence of adaptation by natural selection due to local environmental variation. Yet, the chronology, and mode of the process of parallel evolution remains debated. Here, we harness the temporal resolution of paleogenomics to address these long-standing questions, by comparing genomes originating from the mid-Holocene (8610-5626 years before present, BP) to contemporary pairs of coastal-pelagic ecotypes of bottlenose dolphin. We find that the affinity of ancient samples to coastal populations increases as the age of the samples decreases. We assess the youngest genome (5626 years BP) at sites previously inferred to be under parallel selection to coastal habitats and find it contained coastal-associated genotypes. Thus, coastal-associated variants rose to detectable frequencies close to the emergence of coastal habitat. Admixture graph analyses reveal a reticulate evolutionary history between pelagic and coastal populations, sharing standing genetic variation that facilitated rapid adaptation to newly emerged coastal habitats.

Seasonal changes in diel haul-out patterns of a lacustrine ringed seal (Pusa hispida saimensis).

Seasonal changes in diel haul-out patterns of the lacustrine Saimaa ringed seal (Pusa hispida saimensis) were studied using a combination of satellite telemetry and camera traps during 2007-2015. We found the haul-out activity patterns to vary seasonally. Our results show that during the ice-covered winter period before the seals start their annual molt, the peak in haul-out generally occurs at midnight. Similarly, during the postmolt season of summer and autumn when the lake is free of ice, the haul-out is concentrated in the early hours of the morning. In contrast, over the spring molting period, Saimaa ringed seals tend to haul out around the clock. The spring molt is also the only period when a slight difference in haul-out behavior between the sexes is observed, with females having a haul-out peak at nighttime while the males have a less visible diel pattern. According to our results, the diel haul-out patterns of Saimaa ringed seals are similar to the ones of marine ringed seals. Gathering information on haul-out activity is important in order to safeguard the natural patterns of Saimaa ringed seals in areas that are prone to disturbance from human activities.

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

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.

Seasonal and diel activity patterns of the endangered taiga bean goose (Anser fabalis fabalis) during the breeding season, monitored with camera traps.

Taiga bean goose (Anser fabalis fabalis) is an endangered subspecies that breeds sporadically in remote habitats in the arctic and boreal zones. Due to its elusive behaviour, there is a paucity of knowledge on the behaviour of taiga bean goose during the breeding season, and survey methods for monitoring numbers in the breeding areas are lacking. Camera traps are a useful tool for wildlife monitoring, particularly when there is a need for non-invasive methods due to the shy nature of the species. In this study, we tested the use of camera traps to investigate seasonal and diel activity patterns of taiga bean goose in Finland over two successive breeding seasons, 2018 and 2019. We did this by modelling counts of geese from images with generalized linear and additive mixed models. The camera type (cameras placed by experts specialized in bean goose ecology vs randomly placed cameras) did not influence the count of taiga bean goose (p = 0.386). However, the activity varied significantly by region, Julian day, time of day and temperature, with the study site (individual peatland) and year adding substantial random variation and uncertainty in the counts. Altogether, the best fitting model explained nearly 70% of the variation in taiga bean goose activity. The peak in activity occurred about a month later in the southernmost region compared to the more northern regions, which may indicate behaviours related to migration rather than breeding and moulting. Our results show that long-term monitoring with game camera traps provide a potential unobtrusive approach for studying the behavioural patterns of taiga bean goose and can increase our ecological knowledge of this little-known subspecies. The results can be applied to planning of the annual censuses and finding the optimal time frame for their execution.

Postglacial Colonization of Northern Coastal Habitat by Bottlenose Dolphins: A Marine Leading-Edge Expansion?

Oscillations in the Earth's temperature and the subsequent retreating and advancing of ice-sheets around the polar regions are thought to have played an important role in shaping the distribution and genetic structuring of contemporary high-latitude populations. After the Last Glacial Maximum (LGM), retreating of the ice-sheets would have enabled early colonizers to rapidly occupy suitable niches to the exclusion of other conspecifics, thereby reducing genetic diversity at the leading-edge. Bottlenose dolphins (genus Tursiops) form distinct coastal and pelagic ecotypes, with finer-scale genetic structuring observed within each ecotype. We reconstruct the postglacial colonization of the Northeast Atlantic (NEA) by bottlenose dolphins using habitat modeling and phylogenetics. The AquaMaps model hindcasted suitable habitat for the LGM in the Atlantic lower latitude waters and parts of the Mediterranean Sea. The time-calibrated phylogeny, constructed with 86 complete mitochondrial genomes including 30 generated for this study and created using a multispecies coalescent model, suggests that the expansion to the available coastal habitat in the NEA happened via founder events starting ~15 000 years ago (95% highest posterior density interval: 4 900-26 400). The founders of the 2 distinct coastal NEA populations comprised as few as 2 maternal lineages that originated from the pelagic population. The low effective population size and genetic diversity estimated for the shared ancestral coastal population subsequent to divergence from the pelagic source population are consistent with leading-edge expansion. These findings highlight the legacy of the Late Pleistocene glacial cycles on the genetic structuring and diversity of contemporary populations.

Quantifying dispersal between marine protected areas by a highly mobile species, the bottlenose dolphin, Tursiops truncatus.

The functioning of marine protected areas (MPAs) designated for marine megafauna has been criticized due to the high mobility and dispersal potential of these taxa. However, dispersal within a network of small MPAs can be beneficial as connectivity can result in increased effective population size, maintain genetic diversity, and increase robustness to ecological and environmental changes making populations less susceptible to stochastic genetic and demographic effects (i.e., Allee effect). Here, we use both genetic and photo-identification methods to quantify gene flow and demographic dispersal between MPAs of a highly mobile marine mammal, the bottlenose dolphin Tursiops truncatus. We identify three populations in the waters of western Ireland, two of which have largely nonoverlapping core coastal home ranges and are each strongly spatially associated with specific MPAs. We find high site fidelity of individuals within each of these two coastal populations to their respective MPA. We also find low levels of demographic dispersal between the populations, but it remains unclear whether any new gametes are exchanged between populations through these migrants (genetic dispersal). The population sampled in the Shannon Estuary has a low estimated effective population size and appears to be genetically isolated. The second coastal population, sampled outside of the Shannon, may be demographically and genetically connected to other coastal subpopulations around the coastal waters of the UK. We therefore recommend that the methods applied here should be used on a broader geographically sampled dataset to better assess this connectivity.

Using tagging data and aerial surveys to incorporate availability bias in the abundance estimation of blue sharks (Prionace glauca).

There is worldwide concern about the status of elasmobranchs, primarily as a result of overfishing and bycatch with subsequent ecosystem effects following the removal of top predators. Whilst abundant and wide-ranging, blue sharks (Prionace glauca) are the most heavily exploited shark species having suffered marked declines over the past decades, and there is a call for robust abundance estimates. In this study, we utilized depth data collected from two blue sharks using pop-up satellite archival tags, and modelled the proportion of time the sharks were swimming in the top 1-meter layer and could therefore be detected by observers conducting aerial surveys. The availability models indicated that the tagged sharks preferred surface waters whilst swimming over the continental shelf and during daytime, with a model-predicted average proportion of time spent at the surface of 0.633 (SD = 0.094) for on-shelf, and 0.136 (SD = 0.075) for off-shelf. These predicted values were then used to account for availability bias in abundance estimates for the species over a large area in the Northeast Atlantic, derived through distance sampling using aerial survey data collected in 2015 and 2016 and modelled with density surface models. Further, we compared abundance estimates corrected with model-predicted availability to uncorrected estimates and to estimates that incorporated the average time the sharks were available for detection. The mean abundance (number of individuals) corrected with modelled availability was 15,320 (CV = 0.28) in 2015 and 11,001 (CV = 0.27) in 2016. Depending on the year, these estimates were ~7 times higher compared to estimates without the bias correction, and ~3 times higher compared to the abundances corrected with average availability. When the survey area contains habitat heterogeneity that may affect surfacing patterns of animals, modelling animals' availability provides a robust alternative to correcting for availability bias and highlights the need for caution when applying "average" correction factors.