The Genetic Ecology and Population Origins of the Beluga Whales, Delphinapterus leucas, of Yakutat Bay

Small populations or groups of individuals at the edge of a species’ range can reveal much about a species’ niche preference limitations, its demographic history, and its adaptive potential for range expansion or niche shifts. We investigated whether recent sightings of small numbers (n≤12) of beluga whales, Delphinapterus leucas, in Yakutat Bay, Alaska, some 800 km distant from the nearest known population in Cook Inlet, represented a distinct group of whales or temporary extralimital movements from Cook Inlet, and if the former whether they exhibited any genetic consequences of small effective population size. Using remote biopsy sampling (nsamples=10), mtDNA sequencing, multi-locus genotyping, and PCRbased gender determination, we found that the Yakutat whales comprised both males and females, exhibited site fi delity across years, were signifi cantly differentiated for mtDNA (Fst = 0.54, P < 0.0001) and microsatellite (Fst = 0.10, P < 0.0001) loci from the Cook Inlet population, and formed a distinct genetic cluster. Individual assignment methods identifi ed Cook Inlet as the most likely origin of the Yakutat whales when compared to the four other population stocks in the western Nearctic: Bristol Bay, Norton Sound, the Chukchi Sea, and the Beaufort Sea (n = 494), but individual whales had low likelihoods of coming from Cook Inlet relative to whales sampled in that population. We developed a new exclusion-assignment method, GELATo, that estimates the likelihood of a group of whales arising within one, any, or none of a series of reference populations. Using the same fi ve beluga whale reference populations we confi rmed the close affi nity of Yakutat to Cook Inlet but excluded the Yakutat group as likely immigrants from Cook Inlet (logL= -68.63micros Introduction Individuals on the frontier of a species’ range typically defi ne the geographic limits of suitable conditions for the maintenance of viable populations, but they can also represent the vanguard of a range or niche expansion or the relicts from past retreats. As such, groupings of individuals at the range edge can tell us much about a species’ niche preference limitations, its demographic history, and its adaptability and potential for range expansion or shifts. It is for these reasons that range limits are receiving growing attention in the context of determining how species will face the increasing challenges of environmental and climate change (Gaston, 2009; Sexton et al., 2009, 2011). The geographic range limits of species are often characterized by low population density (Jarema et al., 2009) where populations may be subject to the genetic and demographic consequences of small population size, including negative aspects of inbreeding (Hedrick and Kalinowski, 2000) and the Allee effect (Courchamp et al., 1999). In social species, these effects can be either compounded or alleviated by the size, genetic composition (e.g., kinvs. nonkin-based), and breeding patterns of founding and immigrant groups. Furthermore, the extent of gene fl ow with larger central populations or other edge populations can infl uence the effective population size of marginal populations and the allelic variation upon which selection can act (Sexton et al., 2009, 2011). Thus, determining the genetic origins of marginal populations, their genetic composition and breeding patterns, including levels of relatedness and inbreeding, and the extent of continuing genetic exchange with central populations can provide insight into the factors that infl uence the establishment and persistence of small groups or populations on the geographic frontier of a species’ range. Such insight is key to predicting how species will respond to climate and other environmental change and has immediate application to assessing the viability of core populations, especially those experiencing declines and habitat loss. Beluga whales, Delphinapterus leu cas, have a nonuniform distribution across the Arctic and Subarctic (O’Corry-Crowe, 2008) shaped by and -63.06mtDNA). These fi ndings, in conjunction with recent beluga whale sightings, including young-of-the-year calves, in Yakutat Bay in all seasons, indicate a small, resident, reproductive group with limited current genetic exchange with Cook Inlet. Lower variation (Hobs = 0.580 v. 0.715) at neutral markers, signifi cantly higher relatedness (mean difference in rQeullerGt = 0.410) among and inbreeding (mean difference in F = -0.1 to -0.19) within the Yakutat animals compared to Cook Inlet raise concerns about the loss of genetic diversity over time. While the small size and uncertain history and viability of the Yakutat group creates new management challenges, its location, unique habitat, and persistence up to now can provide insights into the survival of small groups on the warm edge of the species’ range and is a testament to the effective stewardship of the local Tlingit community.