Spatial patterns and rarity of the white‐phased ‘Spirit bear’ allele reveal gaps in habitat protection

Abstract

1. Preserving genetic and phenotypic diversity can help safeguard not only biodiversity but also cultural and economic values. 2. Here, we present data that emerged from Indigenous‐led research at the intersection of evolution and ecology to support conservation planning of a culturally salient, economically valuable, and rare phenotypic variant. We addressed three conservation objectives for the white‐phased ‘Spirit bear’ polymorphism, a rare and endemic white‐coated phenotype of black bear (Ursus americanus) in Kitasoo/Xai'xais and Gitga'at Territories and beyond in coastal British Columbia, Canada. First, we used non‐invasively collected hair samples (n = 385 bears over ∼18,000 km2) to assess the spatial variation in the frequency of the allele that controls the white‐coloured morph (mc1r). Second, we compared our observed allele frequencies at mc1r with those expected under Hardy–Weinberg equilibrium. Finally, we examined how well current protected areas in the region aligned with spatial hotspots of Spirit bear alleles. 3. We found that landscape‐level allele frequency was lower than previously reported. For example our systematic sampling estimated a frequency of 0.25 (95% CI [0.13, 0.41]) on Gribbell Island compared with the previously reported estimate of 0.56. Also, in contrast with previous reports, we failed to detect a statistically significant departure from Hardy–Weinberg equilibrium at mc1r, which calls into question the previously posited role of homozygote gene flow, heterozygote disadvantage, and positive assortative mating in the maintenance of this polymorphism. Finally, we found a discrepancy between the placement of protected areas and the 90th percentile hotspots (upper 10% of all estimated values) of Spirit bear alleles, with ∼50% of hotspots falling outside of protected areas. 4. These results provide new insight into hypotheses related to the maintenance of this rare polymorphism, and directly relevant information to support evidence‐based opportunities for Indigenous Nations of the area to attend to gaps in conservation planning.

Intrapopulation foraging niche variation between phenotypes and genotypes of Spirit bear populations

“…Specifically, given that black bear cubs generally overlap their mother's home range (Rogers, 1987), generations of heterozygote cubs from white mothers could be occupying home ranges at the marine interface. This explanation aligns with the recently reported discrepancy between a shoreline-only sampling program that reported higher G allele frequencies (Ritland et al 2001) compared with a more systematic sampling approach across all elevations (Service et al, 2020). Finally, divergence between black-coated genotypes could be could also be driven by a process previously not identified in the genetic architecture of the polymorphism.…”

“…These samples were subsequently provided to D. Klinka and T. Reimchen by K. Ritland (Klinka, 2004; Reimchen & F I G U R E 1 Study area as defined by the extent of sampled "landmass units" in coastal British Columbia, Canada. Bolded numbers overlaid on select landmass units indicate (where available) the most recent mc1r G allele frequency data (Service et al, 2020) Klinka, 2017), and we used our novel multivariate approach to reexamine the δ 13 C and δ 15 N data from these samples.…”

“…multiniche polymorphism, niche diversity, Spirit bear, Ursus (Ritland et al 2001), though this pattern was not detected in a recent analysis (Service et al, 2020). Differential selection among genotypes that share the same phenotype of coat color has been demonstrated in wolves (Canis lupus; Coulson et al 2011), but the potential role of differences in fitness among genotypes with the same coat color is uncertain in this system.…”

“…Spirit bears coexist with black-coated black bears and have a limited distribution, primarily on several islands and the nearby mainland on the central coast of BC (Marshall & Ritland, 2002;Ritland et al 2001). In this region, frequencies of the Spirit bear phenotype have been estimated as high as 43% (Gribbell Island), but their probability of presence drops to near zero within ~3 km from this concentrated area (Marshall & Ritland, 2002;Ritland et al 2001;Service et al, 2020). Population estimates throughout their distribution vary from ~50 to 500 individuals (Darimont, unpublished data;Blood, 1997;McCrory et al 2001;Sachs, 2010).…”

Old‐growth forest structure in a low‐productivity hypermaritime rainforest in coastal British Columbia, Canada

“…While several studies examining old-growth forest characteristics and gap-forming dynamics have been carried out in warmer and drier rain shadow variants of temperate rainforests located in the Pacific Northwest of the USA Franklin 1988, Spies et al 1990), and in the tall productive (Lertzman et al 1996, Frazer et al 2000) and montane (Parish and Antos 2004) CTR forests of BC, major knowledge gaps remain for the short and slow-growing hypermaritime temperate rainforests located on the outer coast of BC (Kranabetter et al 2003, Mackinnon 2003, Banner et al 2005 (Alaback 1982, Buma et al 2016, Bisbing and Amore 2018, Buma and Thompson 2019), but it is unclear if knowledge from Alaska's hemlock spruce-dominated forest stands are transferable to the cedarhemlock stands of coastal BC. Information on old-growth forest structure in hypermaritime temperate rainforests on the coastal margin of BC is scarce despite their importance for wildlife (Adams et al 2017, Obrist et al 2020, Service et al 2020, soil carbon storage (McNicol et al 2019), and exports of dissolved organic carbon (Oliver et al 2017), which provide energy subsidies to marine environments (St. Pierre et al 2020). These landscapes are characterized by mosaics of wetlands and short-open forests (Thompson et al 2016) and are comprised of long-lived conifer species, yet little is known about species turnover, life histories, and disturbance regimes (Daniels andGray 2006, Alaback et al 2017; but see Banner et al 1983 andBanner 2014).…”