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
Data from: The conservation value of small population remnants: variability in inbreeding depression and heterosis of a perennial herb, the narrow-leaved purple coneflower (Echinacea angustifolia)
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
- PAR ID:
- 10567312
- Publisher / Repository:
- Dryad
- Date Published:
- Subject(s) / Keyword(s):
- habitat fragmentation outbreeding depression multi-year study Aster model genetic rescue Asteraceae FOS: Biological sciences FOS: Biological sciences
- Format(s):
- Medium: X Size: 5610414 bytes
- Size(s):
- 5610414 bytes
- Location:
- Dryad
- Right(s):
- Creative Commons Zero v1.0 Universal
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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
-
Abstract Understanding the genetic and fitness consequences of anthropogenic bottlenecks is crucial for biodiversity conservation. However, studies of bottlenecked populations combining genomic approaches with fitness data are rare. Theory predicts that severe bottlenecks deplete genetic diversity, exacerbate inbreeding depression and decrease population viability. However, actual outcomes are complex and depend on how a species’ unique demography affects its genetic load. We used population genetic and veterinary pathology data, demographic modelling, whole-genome resequencing and forward genetic simulations to investigate the genomic and fitness consequences of a near-extinction event in the northern elephant seal. We found no evidence of inbreeding depression within the contemporary population for key fitness components, including body mass, blubber thickness and susceptibility to parasites and disease. However, we detected a genomic signature of a recent extreme bottleneck (effective population size = 6; 95% confidence interval = 5.0–7.5) that will have purged much of the genetic load, potentially leading to the lack of observed inbreeding depression in our study. Our results further suggest that deleterious genetic variation strongly impacted the post-bottleneck population dynamics of the northern elephant seal. Our study provides comprehensive empirical insights into the intricate dynamics underlying species-specific responses to anthropogenic bottlenecks.more » « less
-
Purugganan, Michael (Ed.)Abstract The deleterious effects of inbreeding have been of extreme importance to evolutionary biology, but it has been difficult to characterize the complex interactions between genetic constraints and selection that lead to fitness loss and recovery after inbreeding. Haploid organisms and selfing organisms like the nematode Caenorhabditis elegans are capable of rapid recovery from the fixation of novel deleterious mutation; however, the potential for recovery and genomic consequences of inbreeding in diploid, outcrossing organisms are not well understood. We sought to answer two questions: 1) Can a diploid, outcrossing population recover from inbreeding via standing genetic variation and new mutation? and 2) How does allelic diversity change during recovery? We inbred C. remanei, an outcrossing relative of C. elegans, through brother-sister mating for 30 generations followed by recovery at large population size. Inbreeding reduced fitness but, surprisingly, recovery from inbreeding at large populations sizes generated only very moderate fitness recovery after 300 generations. We found that 65% of ancestral single nucleotide polymorphisms (SNPs) were fixed in the inbred population, far fewer than the theoretical expectation of ∼99%. Under recovery, 36 SNPs across 30 genes involved in alimentary, muscular, nervous, and reproductive systems changed reproducibly across replicates, indicating that strong selection for fitness recovery does exist. Our results indicate that recovery from inbreeding depression via standing genetic variation and mutation is likely to be constrained by the large number of segregating deleterious variants present in natural populations, limiting the capacity for recovery of small populations.more » « less
-
null (Ed.)Red spruce (Picea rubens Sarg.) is a coniferous tree with a highly fragmented range in eastern North American montane forests. It serves as a foundational species for many locally rare and threatened taxa and has therefore been the focus of large-scale reforestation efforts aimed at restoring these montane ecosystems, yet genetic input guiding these efforts has been lacking. To tackle this issue, we took advantage of a common garden experiment and a whole exome sequencing dataset to investigate the impact of different population genetic parameters on early-life seedling fitness in red spruce. The level of inbreeding, genetic diversity and genetic load were assessed for 340 mother trees sampled from 65 localities across the spe- cies range and compared to different fitness traits measured on 5100 of their seedlings grown in a controlled environment. We identified an overall positive influence of genetic diversity and negative impact of genetic load and population-level inbreeding on early-life fitness. Those associations were most apparent for the highly fragmented populations in the Central and Southern Appalachians, where lower genetic diversity and higher inbreeding were associated with lower germination rate, shorter height and reduced early-life fitness of the seedlings. These results provide unprecedented information that could be used by field managers aiming to restore red spruce forests and to maximize the success of future plantations.more » « less
