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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.
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This content will become publicly available on March 1, 2026
Genomic Insights Into Inbreeding and Adaptive Divergence of Trout Populations to Inform Genetic Rescue
ABSTRACT Genetic rescue, specifically translocation to facilitate gene flow among populations and reduce the effects of inbreeding, is an increasingly used approach in conservation. However, this approach comes with trade‐offs, wherein gene flow may reduce fitness when populations have adaptive differentiation (i.e., outbreeding depression). A better understanding of the interaction between isolation, inbreeding, and adaptive divergence in key traits, such as life history traits, will help to inform genetic rescue efforts. Stream‐dwelling salmonids, such as the westslope cutthroat trout (Oncorhynchus lewisi; WCT), are well‐suited for examining these trade‐offs because they are increasingly isolated by habitat degradation, exhibit substantial variation in life history traits among populations, and include many species of conservation concern. However, few genomic studies have examined the potential trade‐offs in inbreeding versus outbreeding depression in salmonids. We used > 150,000 SNPs to examine genomic variation and inbreeding coefficients in 565 individuals across 25 WCT populations that differed in their isolation status and demographic histories. Analyses of runs of homozygosity revealed that several isolated WCT populations had “flatlined” having extremely low genetic variation and high inbreeding coefficients. Additionally, we conducted genome scans to identify potential outlier loci that could explain life history differences among 10 isolated populations. Genome scans identified one candidate genomic region that influenced maximum length and age‐1 to age‐2 growth. However, the limited number of candidate loci suggests that the life history traits examined may be driven by many genes of small effect or phenotypic plasticity. Although adaptive differentiation should be considered, the high inbreeding coefficients in several populations suggest that genetic rescue may benefit the most genetically depauperate WCT populations.
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- Award ID(s):
- 1652278
- PAR ID:
- 10613573
- Publisher / Repository:
- Evolutionary Applications
- Date Published:
- Journal Name:
- Evolutionary Applications
- Volume:
- 18
- Issue:
- 3
- ISSN:
- 1752-4571
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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
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