4.1 | Inbreeding and demography
Demographic analyses indicate that increased inbreeding in S. catenatus is likely due to decreased population size relative toS. tergenimus over both long-and short term timescales. Over evolutionary timescales (1000’s of years), a coalescent-based PSMC analysis shows that for much of the last 100,000 years S. catenatus has consistently had an effective size that is > 2 – 3X smaller than S. tergeminus even in the face of shifting distributions due to impacts of ice sheet expansion and contraction during the late Pleistocene (Pielou, 1992). Fundamental differences in the ecology of these species may account for the long-term differences in effective size. S. catenatus is a habitat specialist which occupies wetlands or mesic prairie habitats (Szymanski et al., 2016) which are patchily distributed leading to greater population structure and smaller effective sizes (Sovic et al., 2019). In contrast, S. tergeminus is found in more wide-spread continuous xeric grasslands (Stebbins, 1966) and this is reflected in the lack of genetic structure and large effective sizes observed in nature (McClusky & Bender, 2015).
Bottlenecks over recent timescales have also increased inbreeding inS. catenatu s relative to S. tergeminus . The oldest event is most consistent with the timescale of bottlenecks detected by Sovic et al. (2019) and had a proportionally greater impact on S. tergeminus based on the relative abundance of small ROHs in each species. The causes of this decline are unknown seems most likely to be related to large‐scale environmental changes related to climate that have previously been hypothesized to impact the distribution of this (Cook, 1992) and other species in this region of North America (Soltis, Morris, McLachlan, Manos, & Soltis, 2006).
In contrast, we estimate that the two most recent bottleneck events occurred within the last 200 years and the greater relative abundance of both medium and long ROHs in S. catenatus suggest that relative declines in population size have been greater in this species than inS. tergeminus . This timeframe coincides with the colonization and subsequent landscape modification by European settlers in North America (Pielou, 1992; Schmidt, 1938) which has resulted in the habitat destruction and fragmentation that has played a key role in recent range-wide declines of S. catenatus (Szymanski et al., 2016). Overall our analyses provide new historical evidence in support of the idea that anthropogenic impacts have had a consistently greater impact on S. catenatus.
Compared to the species level results, population level comparisons show few significant differences in mean individual FROH and theta between populations. We suggest that this is because all populations have small contemporary effective sizes (Sovic et al., 2019) implying strong inbreeding effects in all populations and high variance in these parameters between individuals within populations (Figure 2a) that reduces statistical power to detect differences. Surprisingly, despite this lack of detectable differences in genome level indications of inbreeding we nonetheless still detect population differences in population specific genetic load (see below). Regardless, our results argue that inbreeding effects in S. catenatus are most strongly manifested at the species rather than the population level.