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1. Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte

   https://doi.org/10.1371/journal.pgen.1009797  

   Samayoa, Luis Fernando; Olukolu, Bode A.; Yang, Chin Jian; Chen, Qiuyue; Stetter, Markus G.; York, Alessandra M.; Sanchez-Gonzalez, Jose de; Glaubitz, Jeffrey C.; Bradbury, Peter J.; Romay, Maria Cinta; et al (December 2021, PLOS Genetics)

   Walsh, Bruce (Ed.)

   Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to large-effect mutations versus variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load in the maize population that we predicted from sequence data. Parental breeding values were highly consistent between outcross and selfed offspring, indicating that additive effects determine most of the genetic value even in the presence of strong inbreeding depression. We developed a novel linkage scan to identify quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, small-effect partially recessive effects in linkage disequilibrium underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against some large effect variants, but polygenic load is harder to purge and overall segregating mutational burden increased in maize compared to teosinte. 

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2. Severe inbreeding, increased mutation load and gene loss-of-function in the critically endangered Devils Hole pupfish

   https://doi.org/10.1098/rspb.2022.1561  

   Tian, David; Patton, Austin H.; Turner, Bruce J.; Martin, Christopher H. (November 2022, Proceedings of the Royal Society B: Biological Sciences)

   Small populations with limited range are often threatened by inbreeding and reduced genetic diversity, which can reduce fitness and exacerbate population decline. One of the most extreme natural examples is the Devils Hole pupfish ( Cyprinodon diabolis ), an iconic and critically endangered species with the smallest known range of any vertebrate. This species has experienced severe declines in population size over the last 30 years and suffered major bottlenecks in 2007 and 2013, when the population shrunk to 38 and 35 individuals, respectively. Here, we analysed 30 resequenced genomes of desert pupfishes from Death Valley, Ash Meadows and surrounding areas to examine the genomic consequences of small population size. We found extremely high levels of inbreeding ( F ROH = 0.34–0.81) and an increased amount of potentially deleterious genetic variation in the Devils Hole pupfish as compared to other species, including unique, fixed loss-of-function alleles and deletions in genes associated with sperm motility and hypoxia. Additionally, we successfully resequenced a formalin-fixed museum specimen from 1980 and found that the population was already highly inbred prior to recent known bottlenecks. We thus document severe inbreeding and increased mutation load in the Devils Hole pupfish and identify candidate deleterious variants to inform management of this conservation icon. 

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3. The conservation value of small population remnants: Variability in inbreeding depression and heterosis of a perennial herb, the narrow-leaved purple coneflower (Echinacea angustifolia)

   https://doi.org/10.1093/jhered/esae055  

   Thoen, Riley D; Southgate, Andrea; Kiefer, Gretel; Shaw, Ruth G; Wagenius, Stuart (October 2024, Journal of Heredity)

   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. 

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4. Experimental evidence of inbreeding depression for competitive ability and its population-level consequences in a mixed-mating plant

   https://doi.org/10.3389/fpls.2024.1398060  

   Walker, Mark J; Spigler, Rachel B (September 2024, Frontiers in Plant Science)

   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. 

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5. 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)

   https://doi.org/10.5061/dryad.zcrjdfnp2  

   Thoen, Riley; Southgate, Andrea; Kiefer, Gretel; Shaw, Ruth; Wagenius, Stuart (January 2024, Dryad)

   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