An official website of the United States government
Anthropogenically fragmented populations may have reduced fitness due to loss of genetic diversity and inbreeding. The extent of such fitness losses due to fragmentation and potential gains from conservation actions are infrequently assessed together empirically. Controlled crosses within and among populations can identify whether populations are at risk of inbreeding depression and whether inter-population crossing alleviates fitness loss. Because fitness depends on the environment and life stage, studies quantifying cumulative fitness over a large portion of the lifecycle in conditions that mimic natural environments are most informative. To assess the fitness consequences of habitat fragmentation, we leveraged controlled within-family, within-population, and between-population crosses to quantify inbreeding depression and heterosis in seven populations of Echinacea angustifolia within a 6,400-ha area. We then assessed cumulative offspring fitness after 14 yr of growth in a natural experimental plot (N = 1,136). The mean fitness of progeny from within-population crosses varied considerably, indicating genetic differentiation among source populations, even though these sites are all less than 9 km apart. The fitness consequences of within-family and between-population crosses varied in magnitude and direction. Only one of the seven populations showed inbreeding depression of high effect, while four populations showed substantial heterosis. Outbreeding depression was rare and slight. Our findings indicate that local crossings between isolated populations yield unpredictable fitness consequences ranging from slight decreases to substantial increases. Interestingly, inbreeding depression and heterosis did not relate closely to population size, suggesting that all fragmented populations could contribute to conservation goals as either pollen recipients or donors.
more »
« less
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 multigenerational 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.
more »
« less
- Award ID(s):
- 2016569
- PAR ID:
- 10660589
- Publisher / Repository:
- PNAS
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 122
- Issue:
- 34
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- e2501745122
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Anthropogenically fragmented populations may have reduced fitness due to loss of genetic diversity and inbreeding. The extent of such fitness losses due to fragmentation and potential gains from conservation actions are infrequently assessed together empirically. Controlled crosses within and among populations can identify whether populations are at risk of inbreeding depression and whether interpopulation crossing alleviates fitness loss. Because fitness depends on environment and life stage, studies quantifying cumulative fitness over a large portion of the lifecycle in conditions that mimic natural environments are most informative. To assess fitness consequences of habitat fragmentation, we leveraged controlled within-family, within-population, and between-population crosses to quantify inbreeding depression and heterosis in seven populations of Echinacea angustifolia within a 6400-hectare area. We then assessed cumulative offspring fitness after 14 years of growth in a natural experimental plot (N = 1136). Mean fitness of progeny from within-population crosses varied considerably, indicating genetic differentiation among source populations, even though these sites are all less than 9 km apart. The fitness consequences of within-family and between-population crosses varied in magnitude and direction. Only one of the seven populations showed inbreeding depression of high effect, while four populations showed substantial heterosis. Outbreeding depression was rare and slight. Our findings indicate that local crossings between isolated populations yield unpredictable fitness consequences ranging from slight decreases to substantial increases. Interestingly, inbreeding depression and heterosis did not relate closely to population size, suggesting that all fragmented populations could contribute to conservation goals as either pollen recipients or donors.more » « less
-
Inbreeding depression is a key factor regulating the evolution of self-fertilization in plants. Despite predictions that inbreeding depression should evolve with selfing rates as deleterious alleles are increasingly exposed and removed by selection, evidence of purging the genetic load in wild populations is equivocal at best. This discordance could be explained, in part, if the load underlying inbreeding depression is subject to soft selection, i.e., the fitness of selfed individuals depends on the frequency and density of selfed vs. outcrossed individuals in the population. Somewhat counterintuitively, this means that populations with contrasting mutation load can have similar fitness. Soft selection against selfed individuals may be expected when there is inbreeding depression for competitive ability in density-regulated populations. We tested population-level predictions of inbreeding depression in competitive ability by creating a density series of potted plants consisting of either purely outcrossed, purely selfed, or mixed (50% outcrossed, 50% selfed) seed of the mixed-mating biennialSabatia angularis(Gentianaceae) representing ecological neighborhoods. Focusing on the growth and survival of juveniles, we show that mean plant size is independent of neighborhood composition when resources are limiting, but greatest in outcrossed neighborhoods at low densities. Across a range of densities, this manifests as stronger density-dependence in outcrossed populations compared to selfed or mixed ones. We also found significantly greater size inequalities among individuals in mixed neighborhoods, even at high densities where mean juvenile size converged, a key signature of asymmetric competition between outcrossed and selfed individuals. Our work illustrates how soft selection could shelter the genetic load underlying inbreeding depression and its demographic consequences.more » « less
-
The persistence of small populations is influenced by the degree and cost of inbreeding, with the degree of inbreeding depending on whether close-kin mating is passively or actively avoided. Few studies have simultaneously studied these factors. We examined inbreeding in a small, isolated population of westslope cutthroat trout using extensive genetic and demographic data. Passive inbreeding avoidance was low, with predicted lifetime dispersal of approximately 36 and 74 m for females and males, respectively. Additionally, we found limited evidence for active inbreeding avoidance during reproduction. Relatives remained spatially clustered into adulthood, and observed relatedness among mate pairs was greater than expected under random mating by 0.09, suggesting that inbreeding is a concern in this population. Further, we examined sex-specific inbreeding depression throughout the life cycle and provide evidence for inbreeding depression in some fitness components, including family size, juvenile survival and reproductive success. Our results suggest that, in an at-risk trout population, limited passive and active inbreeding avoidance lead to a higher degree of inbreeding than expected under random mating. Observed inbreeding, along with evidence for fitness reduction due to inbreeding depression, could put the population at a heightened risk of decline or extirpation.more » « less
-
Anthropogenic destruction and fragmentation of habitat restrict many species to small, isolated populations, which often experience high extirpation risk. Restoring connectivity through translocations is one approach for mitigating the demographic and genetic perils faced by small populations. However, translocation interventions often lack substantial postrelease monitoring, and thus important information including the performance of translocated individuals, the long-term impacts on the recipient population, and the extent to which management objectives are fulfilled over time are often poorly known. Here, we examined the establishment dynamics and long-term outcomes of translocations from multiple donor populations into an intensively monitored population of the federally threatened red-cockaded woodpecker. We found evidence that translocations contributed to population growth and led to genetic admixture within the population. The translocated birds provided direct demographic benefits through high rates of establishment, breeding, and survival. We found that the survival and lifetime reproductive success of individuals were positively related to their amount of translocation ancestry, indicating that demographic benefits extended beyond the direct performances of the translocated birds. The translocations diversified the population’s genetic composition with the ancestry of most individuals in the latter years of the study deriving from multiple translocation donor populations. We found marked heterogeneity in the genetic contributions of translocated individuals and cohorts, leading to disproportionate representation of certain lineages. Encouragingly, despite some accumulation of inbreeding during the study, the translocations thus far have not substantially contributed to inbreeding. Our findings illustrate in precise detail how translocations can be an effective approach for managing imperiled taxa.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1073/pnas.2501745122
