An official website of the United States government
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
Interpopulation variation in inbreeding is primarily driven by tolerance of mating with relatives in a spermcasting invertebrate
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
- Award ID(s):
- 2109676
- PAR ID:
- 10443466
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Evolutionary Biology
- Volume:
- 36
- Issue:
- 1
- ISSN:
- 1010-061X
- Format(s):
- Medium: X Size: p. 95-108
- Size(s):
- p. 95-108
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT Increased parental relatedness occurs in small wild populations and in closed colonies in captivity and reduces offspring fitness. A closed colony ofPeromyscus maniculatusis maintained as genetically diverse stock at the Peromyscus Genetic Stock Center since 1963. Breeding records are available for all the years of breeding in captivity, which allows evaluation of the breeding performance since the inception of the stock. Kinship calculations showed that increased parental relatedness results in offspring loss, which is consistent with the operation of inbreeding depression and is common in small populations, both wild and captive. Nonetheless, an adaptive response was recorded that mitigated the adverse consequences of inbreeding and contributed to the long‐term stability of the colony: When parental relatedness increased, more offspring were produced, resulting in the overall number of viable offspring being unaffected. The underlying mechanism involved adjustments in the interval for mating between related parents, causing the production of more litters. These adaptive changes indicate that the harmful consequences of inbreeding may be partially relieved by mechanisms involving changes in the animals' reproductive strategy. The availability of the breeding records ofP. maniculatusenables the performance of additional studies asking different questions regarding the breeding dynamics of a closed colony under regulated conditions.more » « less
-
Abstract The abundance of many Caribbean corals has declined over the past few decades, yet nowPorites astreoidesis more common on many shallow reefs than in the 1980s and shows evidence of local adaptation. We compare the small‐scale (1–8000 m) genetic structure of this brooding species and the broadcasting coralOrbicella annularison reefs (<14 m depth) in St. John, US Virgin Islands, to examine how larval dispersal and asexual propagation contribute to the retention of genotypes within reefs. Populations ofP. astreoideshave genetic structure across reefs separated by a few 100 m, increased relatedness within reefs, and parthenogenetic larval propagation confirmed by parent–offspring genotyping. Within reefs,P. astreoidescolonies <1 m apart are more related, independent of clonal reproduction, than corals at greater distances. In contrast,O. annularislacks across‐reef genetic structure, has low relatedness within and among reefs, and does not produce asexual larvae. Small‐scale genetic structure and high relatedness inP. astreoidesare evident even without considering asexual propagation, but asexual reproduction enhances these differences. Neither species shows the genetic signature of inbreeding or reduced genotypic diversity despite the high within‐site relatedness ofP. astreoides. Monitoring on these reefs from 1987 indicates thatPoriteshas increased in abundance whileOrbicellahas decreased in abundance. The success ofPoritesis due to greatly increased settlement and recruitment compared withOrbicella. Together these results indicate that high numbers of locally retained and successful genotypes might explain the relative success ofPoriteson shallow, present‐day reefs in the Caribbean.more » « less
-
AbstractInsect societies vary greatly in their social structure, mating biology, and life history. Polygyny, the presence of multiple reproductive queens in a single colony, and polyandry, multiple mating by females, both increase the genetic variability in colonies of eusocial organisms, resulting in potential reproductive conflicts. The co-occurrence of polygyny and polyandry in a single species is rarely observed across eusocial insects, and these traits have been found to be negatively correlated in ants.Acromyrmexleaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South AmericanAcromyrmexspecies to study how different selective pressures influence the evolution of polygyny and polyandry. We show thatAcromyrmexspecies exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species,Acromyrmex lobicornis, displays a significantly lower mating frequency compared to others, while another species,A. lundii, appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution inAcromyrmexleaf-cutting ants. Significance statementMany species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.more » « less
-
null (Ed.)Climate change is resulting in warmer temperatures that are negatively impacting corals. Understanding how much individuals within a population vary in their thermal tolerance and whether this variation is heritable is important in determining whether a species can adapt to climate change. To address this, Acropora cervicornis fragments from 20 genetically distinct colonies collected from the Coral Restoration Foundation Tavernier nursery (Florida, USA) were kept at either ambient (28 ± 1°C) or elevated (32 ± 1°C) temperatures, and mortality was monitored for 26 d. Both broad-sense ( H 2 ) and narrow-sense ( h 2 ) heritability of thermal tolerance were estimated to determine the amount of genetic variation underlying survival to elevated temperature. To understand the physiological basis of thermal tolerance, tissue from both treatments was taken 12 h after the start of the experiment to investigate gene expression at the mRNA and protein level between tolerant and susceptible colonies. Results revealed that this population has considerable total genetic variation in thermal tolerance ( H 2 = 0.528), but low variance in relatedness among colonies prevented us from making any conclusions regarding h 2 . Despite high transcriptomic variability among and within colonies, 40 genes were consistently and significantly different between tolerant and susceptible colonies, and could be potential biomarkers for thermal tolerance should they be verified in a larger sample. Overall, the results suggest that this population has substantial genetic variation for traits that directly impact thermal tolerance; however, their response to projected increases in temperature will depend on more precise estimates of the additive components of this variation ( h 2 ).more » « less
