Inbreeding reduces fitness in spatially structured populations of a threatened rattlesnake

Small and fragmented populations are at high risk of local extinction, in
part because of elevated inbreeding and subsequent inbreeding depression.
A major conservation priority is to identify the mechanisms and extent of
inbreeding depression in small populations. The eastern massasauga
(Sistrurus catenatus) rattlesnake is listed as Federally Threatened in the
United States, having experienced significant habitat fragmentation and
concomitant population declines over the past 200 years. Here, we use
long-term monitoring of two wild populations of eastern massasaugas in
Michigan to estimate the extent of inbreeding in each population, identify
mechanisms that generate inbreeding, and test for the impact of inbreeding
on fitness. Using targeted genomic data and spatial coordinates of capture
locations from over 1000 individuals, we find evidence of inbreeding and
link inbreeding to spatial kinship structure within populations, possibly
driven by limited dispersal. We reconstruct multi-generational pedigrees
for each population to measure reproductive output and use long-term
capture-recapture data to estimate individual survival (i.e., the two
major components of fitness). We find evidence of inbreeding depression in
both fitness metrics. The 5% most inbred individuals are 13.5% less likely
to have any surviving offspring and have 11.6% lower annual survival
compared to all less inbred individuals. By combining genomics and
long-term monitoring data, we are able to link the life history of eastern
massasaugas to inbreeding and detect relationships between fitness and
inbreeding. These insights provide important conservation context for
future management and for understanding how spatial structure can generate
inbreeding depression even at fine spatial scales.