An official website of the United States government
Abstract Meta‐studies on hermaphrodites have found a negative relationship between primary selfing rates and levels of inbreeding depression (ID) and, thus, generally support purging in inbred systems. However, in plants, high among‐taxa variance in ID results in no difference in the mean ID between outcrossing and mixed‐mating taxa. Selective interference likely explains high ID among mixed‐mating taxa, whereas low levels of ID among mixed‐mating taxa are not as stressed. Among animal hermaphrodites, primarily molluscs, there are little data on mixed‐mating systems. To fill a taxonomic and mating system gap, we tested for ID in a mixed‐mating tapeworm,Oochoristica javaensis. We provide a direct estimate of ID across infection of an intermediate host by comparing selfing rates at two life history stages. We found little to no evidence for ID, and the level of ID falls in line with what is reported for highly selfing species even thoughO. javaensishas mixed mating. We discuss this result within the context of kin mating inO. javaensis. Our results emphasize that primary selfing rates alone may be insufficient to classify the inbreeding history in all species when testing for a relationship to ID. Mixed‐mating taxa, and possibly some outcrossing taxa, may exhibit low levels of ID if biparental inbreeding is also driving purging. We advocate that ID studies report estimates of inbreeding history (e.g.FISor identity disequilibrium) from nature‐derived adult samples to provide context rather than relying on primary selfing rates alone.
more »
« less
Testing the Mating System Model of Parasite Complex Life Cycle Evolution Reveals Demographically Driven Mixed Mating
Many parasite species use multiple host species to complete development; however, empirical tests of models that seek to understand factors impacting evolutionary changes or maintenance of host number in parasite life cycles are scarce. Specifically, Brown et al.’s (2001) mating system model, which posits multi-host life cycles are an adaptation to prevent inbreeding in hermaphroditic parasites and thus, preclude inbreeding depression, remains untested. The model assumes loss of a host results in parasite inbreeding and predicts host loss can only evolve if there is no parasite inbreeding depression. We provide the first empirical tests of this model using a novel approach we developed for assessing inbreeding depression from field-collected, parasite samples. The method compares genetically-based, selfing-rate estimates to a demographic-based selfing rate, which was derived from the closed mating system experienced by endoparasites. Results from the hermaphroditic trematode Alloglossidium renale, which has a derived 2-host life cycle, supported both the assumption and prediction of the mating system model as this highly inbred species had no indication of inbreeding depression. Additionally, comparisons of genetic and demographic selfing rates revealed a mixed mating system that could be explained completely by the parasite’s demography, i.e., its infection intensities.
more »
« less
- Award ID(s):
- 1655147
- PAR ID:
- 10547191
- Publisher / Repository:
- The University of Chicago Press
- Date Published:
- Journal Name:
- The American Naturalist
- ISSN:
- 0003-0147
- Page Range / eLocation ID:
- 000 to 000
- Subject(s) / Keyword(s):
- selfing rate inbreeding depression trematode hermaphrodite precocious development infection intensity parasite helminth complex life cycle
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
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 maintenance of males at intermediate frequencies is an important evolutionary problem. Several species of Caenorhabditis nematodes have evolved a mating system in which selfing hermaphrodites and males coexist. While selfing produces XX hermaphrodites, cross-fertilization produces 50% XO male progeny. Thus, male mating success dictates the sex ratio. Here, we focus on the contribution of the male secreted short (mss) gene family to male mating success, sex ratio, and population growth. The mss family is essential for sperm competitiveness in gonochoristic species, but has been lost in parallel in androdioecious species. Using a transgene to restore mss function to the androdioecious Caenorhabditis briggsae, we examined how mating system and population subdivision influence the fitness of the mss+ genotype. Consistent with theoretical expectations, when mss+ and mss-null (i.e., wild type) genotypes compete, mss+ is positively selected in both mixed-mating and strictly outcrossing situations, though more strongly in the latter. Thus, while sexual mode alone affects the fitness of mss+, it is insufficient to explain its parallel loss. However, in genetically homogenous androdioecious populations, mss+ both increases male frequency and depresses population growth. We propose that the lack of inbreeding depression and the strong subdivision that characterize natural Caenorhabditis populations impose selection on sex ratio that makes loss of mss adaptive after self-fertility evolves.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
-
Abstract The degree to which individuals inbreed is a fundamental aspect of population biology shaped by both passive and active processes. Yet, the relative influences of random and non‐random mating on the overall magnitude of inbreeding are not well characterized for many taxa. We quantified variation in inbreeding among qualitatively accessible and isolated populations of a sessile marine invertebrate (the colonial ascidianLissoclinum verrilli) in which hermaphroditic colonies cast sperm into the water column for subsequent uptake and internal fertilization. We compared estimates of inbreeding to simulations predicting random mating within sites to evaluate if levels of inbreeding were (1) less than expected because of active attempts to limit inbreeding, (2) as predicted by genetic subdivision and passive inbreeding tolerance, or (3) greater than simulations due to active attempts to promote inbreeding via self‐fertilization or a preference for related mates. We found evidence of restricted gene flow and significant differences in the genetic diversity ofL. verrillicolonies among sites, indicating that on average colonies were weakly related in accessible locations, but their levels of relatedness matched that of first cousins or half‐siblings on isolated substrates. Irrespective of population size, progeny arrays revealed variation in the magnitude of inbreeding across sites that tracked with the mean relatedness of conspecifics. Biparental reproduction was confirmed in most offspring (86%) and estimates of total inbreeding largely overlapped with simulations of random mating, suggesting that interpopulation variation in mother–offspring resemblance was primarily due to genetic subdivision and passive tolerance of related mates. Our results highlight the influence of demographic isolation on the genetic composition of populations, and support theory predicting that tolerance of biparental inbreeding, even when mates are closely related, may be favoured under a broad set of ecological and evolutionary conditions.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1086/732807
