Relative effects of nocturnal vs diurnal pollinators and distance on gene flow in small Silene alba populations

Silene alba exists in natural metapopulations throughout its range and is visited by a suite of both diurnal and nocturnal pollinators. Pollen-mediated gene flow may help reduce genetic isolation of subpopulations. Here, we compared the relative effects of nocturnal vs diurnal pollinators on pollen-mediated gene flow in subpopulations separated by two distance treatments. We established populations consisting of genetically marked individuals in an old field in Tennessee (USA). Electrophoretic examination of seedlings produced by plants exposed to nocturnal, diurnal and control pollinator treatments and separated by either 20 or 80 m allowed us to directly measure pollen-mediated gene flow. Gene flow was more common between populations separated by only 20 m. Nocturnal pollinators were responsible for most gene flow between populations, regardless of distance. Diurnal pollinators played only a small role in pollen-mediated gene flow. The results suggest that nocturnal pollinators are better than diurnal pollinators at moving pollen between small S. alba subpopulations. However, their effectiveness declines as the distance between subpopulations increases, making them relatively ineffective at moving genes between isolated subpopulations.     

Conservation genetics of the wood ant, Formica lugubris, in a fragmented landscape

Various intrinsic factors connected to the special features of sociality influence the persistence of social insect populations, including low effective population size, reduced amount of genetic variation easily leading to inbreeding depression, and spatially structured populations. In this work, we studied an isolated, small and fragmented population system of the red wood ant Formica lugubris, and evaluated the impact of social and genetic population structure on the persistence and conservation of the populations. The effective population size was large in our study population because all nests were polygynous. As a result, and despite the apparent isolation, the amount of nuclear genetic variability was similar to that in a nonisolated population system. Lack of inbreeding, as well as a high level of variability, indirectly suggests that this population does not suffer from inbreeding depression. The spatial distribution of genetic variation between local populations suggests intensive, but strongly male-biased, nuclear gene flow. Thus, the persistence of this population system does not seem to be threatened by any immediate social or genetic factor, but colonization of new habitat patches may be difficult because of restricted female dispersal.     

Inbreeding depression and heterosis in a subdivided population: influence of the mating system

We investigate the joint effects of gene flow and selfing on the level of inbreeding depression, heterosis and genetic load in a subdivided population at equilibrium. Low gene flow reduces inbreeding depression and substantially increases heterosis. However, in highly self-fertilizing populations, inbreeding depression is independent of the amount of gene flow. When migration occurs via pollen, consanguinity of the reproductive system could have a negative influence on subpopulation persistence, in contrast to the case of isolated populations. However, with only seed migration, genetic load and heterosis depend mildly on the mating system. From an evolutionary point of view, we reach two main conclusions: first, outcrossing is selected for if gene flow is low; second, intermediate levels of gene flow could promote mixed mating systems, especially when migration occurs through pollen.     

Inbreeding and disease avoidance in a free‐ranging koala population

Habitat destruction and fragmentation are increasing globally, forcing surviving species into small, isolated populations. Isolated populations typically experience heightened inbreeding risk and associated inbreeding depression and population decline; although individuals in these populations may mitigate these risks through inbreeding avoidance strategies. For koalas, as dietary specialists already under threat in the northern parts of their range, increased habitat fragmentation and associated inbreeding costs are of great conservation concern. Koalas are known to display passive inbreeding avoidance through sex‐biased dispersal, although population isolation will reduce dispersal pathways. We tested whether free‐ranging koalas display active inbreeding avoidance behaviours. We used VHF tracking data, parentage reconstruction, and veterinary examination results to test whether free‐ranging female koalas avoid mating with (a) more closely related males; and (b) males infected with sexually transmitted Chlamydia pecorum. We found no evidence that female koalas avoid mating with relatively more related available mates. In fact, as the relatedness of potential mates increases, so did inbreeding events. We also found no evidence that female koalas can avoid mating with males infected with C. pecorum. The absence of active inbreeding avoidance mechanisms in koalas is concerning from a conservation perspective, as small, isolated populations may be at even higher risk of inbreeding depression than expected. At risk koala populations may require urgent conservation interventions to augment gene flow and reduce inbreeding risks. Similarly, if koalas are not avoiding mating with individuals with chlamydial disease, populations may be at higher risk from disease than anticipated, further impacting population viability.     

Limited male dispersal in a social spider with extreme inbreeding

Cooperatively breeding animals commonly avoid incestuous mating through pre-mating dispersal. However, a few group-living organisms, including the social spiders, have low pre-mating dispersal, intra-colony mating, and inbreeding. This results in limited gene flow among colonies and sub-structured populations. The social spiders also exhibit female-biased sex ratios because survival benefits to large colonies favour high group productivity, which selects against 1 : 1 sex ratios. Although propagule dispersal of mated females may occasionally bring about limited gene flow, little is known about the role of male dispersal. We assessed the extent of male movement between colonies in natural populations both experimentally and by studying colony sex ratios over the mating season. We show that males frequently move to neighbouring colonies, whereas only 4% of incipient nests were visited by dispersing males. Neighbouring colonies are genetically similar and movement within colony clusters does not contribute to gene flow. Post-mating sex ratio bias was high early in the mating season due to protandry, and also in colonies at the end of the season, suggesting that males remain in the colony when mated females have dispersed. Thus, male dispersal is unlikely to facilitate gene flow between different matrilineages. This is consistent with models of non-Fisherian group-level selection for the maintenance of female biased sex ratios, which predict the elimination of male dispersal.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society 2009, 97 , 227–234.     

Inbreeding and inbreeding depression in a threatened endemic plant,the African violet (Saintpaulia ionantha ssp. grotei), of the East Usambara Mountains,Tanzania

Mating among closely‐related individuals in small and isolated plant populations may result in reduced vigour of the inbred offspring, i.e. inbreeding depression, especially in naturally outbreeding plants. Occurrence of inbreeding and inbreeding depression was studied in Saintpaulia ionantha ssp. grotei, a threatened endemic plant species with a narrow ecological amplitude from the East Usambara Mountains. The level of inbreeding (measured as the fixation index, F) was investigated in twelve populations by analyzing variation at one microsatellite marker locus. The effect of one generation of selfing and outcrossing on the progeny fitness was studied by controlled crosses in two small patches that differ in the level isolation. The fixation index (F) across the populations was on the average 0.21 and varied among the populations from substantial inbreeding (F = 0.58) to surplus heterozygosity (F = −0.29). High inbreeding depression (δ) was observed at early and late stages of the life‐cycle. The isolated patch exhibited lower inbreeding depression than did the non‐isolated patch. The results of this study suggest that inbreeding and subsequent inbreeding depression are potential threats to the survival of Saintpaulia populations.     

Interpopulation variation in inbreeding is primarily driven by tolerance of mating with relatives in a spermcasting invertebrate

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 ascidian Lissoclinum 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 of L. verrilli colonies 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.     

Low level of pollen-mediated gene flow from cultivated to wild grapevine: consequences for the evolution of the endangered subspecies Vitis vinifera L. subsp. silvestris

A parentage and a paternity-based approach were tested for estimation of pollen-mediated gene flow in wild grapevine (Vitis vinifera L. subsp. silvestris), a wind-pollinated species occurring in Mediterranean Europe and southwestern Asia. For this purpose, 305 seedlings collected in 2 years at 2 locations in France from 4 wild female individuals and 417 wild individuals prospected from France and Italy were analyzed using 20 highly polymorphic microsatellite loci. Their profiles were compared with a database consisting of 3203 accessions from the Institut National de la Recherche Agronomique Vassal collection including cultivars, rootstocks, interspecific hybrids, and other wild individuals. Paternity was assigned for 202 (66.2%) of the 305 seedlings, confirming the feasibility of the method. Most of the fertilizing pollen could be assigned to wild males growing nearby. Estimates of pollen immigration from the cultivated compartment (i.e., the totality of cultivars) ranged from 4.2% to 26% from nearby vineyards and from hidden pollinators such as cultivars and rootstocks that had escaped from farms. In an open landscape, the pollen flow was correlated to the distance between individuals, the main pollinator being the closest wild male (accounting for 51.4-86.2% of the pollen flow). In a closed landscape, more complex pollination occurred. Analysis of the parentage of the 417 wild individuals also revealed relationships between nearby wild individuals, but in the case of 12 individuals (3%), analysis revealed pollen immigration from vineyards, confirming the fitness of the hybrid seedlings. These pollen fluxes may have a significant effect on the evolution of wild populations: on the one hand, the low level of pollen-mediated gene flow from cultivated to wild grapevine could contribute to a risk of extinction of the wild compartment (i.e., the totality of the wild individuals). On the other hand, pollen dispersal within the wild populations may induce inbreeding depression of wild grapevines.     

Ancestral inbreeding reduces the magnitude of inbreeding depression in Drosophila melanogaster

The influence of natural selection on the magnitude of inbreeding depression is an important issue in conservation biology and the study of evolution. It is generally expected that the magnitude of inbreeding depression in small populations will depend upon the average homozygosity of individuals, as measured by the coefficient of inbreeding (F). However, if deleterious recessive alleles are selectively purged from populations during inbreeding, then inbreeding depression may differ among populations in which individuals have the same inbreeding coefficient. In such cases, the magnitude of inbreeding depression will partly depend on the ancestral inbreeding coefficient (fa), which measures the cumulative proportion of loci that have historically been homozygous and therefore exposed to natural selection. We examined the inbreeding depression that occurred in lineages of Drosophila melanogaster maintained under pedigrees that led to the same inbreeding coefficient (F = 0.375) but different levels of ancestral inbreeding (fa = 0.250 or 0.531). Although inbreeding depression varied substantially among individual lineages, we observed a significant 40% decrease in the median level of inbreeding depression in the treatment with higher ancestral inbreeding. Our results demonstrate that high levels of ancestral inbreeding are associated with greater purging effects, which reduces the inbreeding depression that occurs in isolated populations of small size.     

Determinants of extinction in fragmented plant populations: Crepis sancta (asteraceae) in urban environments

Local populations are subject to recurrent extinctions, and small populations are particularly prone to extinction. Both demographic (stochasticity and the Allee effect) and genetic factors (drift load and inbreeding depression) potentially affect extinction. In fragmented populations, regular dispersal may boost population sizes (demographic rescue effect) or/and reduce the local inbreeding level and genetic drift (genetic rescue effect), which can affect extinction risks. We studied extinction processes in highly fragmented populations of the common species Crepis sancta (Asteraceae) in urban habitats exhibiting a rapid turnover of patches. A four-year demographic monitoring survey and microsatellite genotyping of individuals allowed us to study the determinants of extinction. We documented a low genetic structure and an absence of inbreeding (estimated by multilocus heterozygosity), which suggest that genetic factors were not a major cause of patch extinction. On the contrary, local population size was the main factor in extinction, whereas connectivity was shown to decrease patch extinction, which we interpreted as a demographic rescue effect that was likely due to better pollination services for reproduction. This coupling of demographic and genetic tools highlighted the importance of dispersal in local patch extinctions of small fragmented populations connected by gene flow.     

Testing for stress-dependent inbreeding depression in Impatiens capensis (Balsaminaceae)

The relevance of inbreeding depression to the persistence of plant populations can depend upon whether stress magnifies inbreeding depression for fitness-related traits. To examine whether drought stress exacerbates inbreeding depression in gas exchange traits and biomass, we grew selfed and outcrossed progeny of inbred lines from two populations of Impatiens capensis in a greenhouse experiment under water-limited and moist soil conditions. Drought stress did not magnify the degree of inbreeding depression for any of the traits measured. In fact, in one population there was a trend for stronger inbreeding depression under well-watered, benign conditions. Furthermore, significant inbreeding depression for carbon assimilation rate and stomatal conductance was only detected in the lines from one population. In contrast, inbreeding depression for biomass was detected within both populations and differed among lines. Drought stress exerted significant selection on physiological traits, favoring increased carbon assimilation rates and decreased stomatal conductance in drought-stressed plants. Patterns of selection did not differ between inbred and outcrossed plants but did differ marginally between populations. Thus, estimates of selection were not biased by the mixed mating system per se, but may be biased by combining individuals from populations with different histories of selection and inbreeding.     

Allozyme Variation in the Rare Gulf Coast Endemic Polygonella macrophylla Small (Polygonaceae)

Abstract Polygonella macrophylla Small is a rare, perennial, primarily gynodioecious plant species endemic to a narrow zone of coastal sand pine scrub habitat along the Gulf of Mexico from Carrabelle, Florida, to Gulf Shores, Alabama (U.S.A.). The species is comprised of a crimson-red flowered form ("rubra"), known from only two populations at the eastern distributional limit of the species, and a white/pink flowered form ("alba") represented by several populations throughout the remainder of the range of the species. An electrophoretic investigation revealed that commonly used measures of gene diversity are very close to expected values in "rubra" given the combination of ecological attributes displayed by the species; however, gene diversity in "alba" is much lower than expected. Population differentiation is high, with estimates of the coefficient of gene differentiation ( G _ST ) indicating that more than 30% of the diversity is among populations. Lack of gene flow among populations, estimated to be at most 0.6 migrating individuals per generation for the species, is a likely cause of greater population differentiation. High inbreeding, detected both within populations and within the species, is suggestive of high rates of self-fertilization in hermaphroditic plants and/or biparental inbreeding in small populations.     

Genetic evidence for landscape effects on dispersal in the army ant Eciton burchellii

Inhibited dispersal, leading to reduced gene flow, threatens populations with inbreeding depression and local extinction. Fragmentation may be especially detrimental to social insects because inhibited gene flow has important consequences for cooperation and competition within and among colonies. Army ants have winged males and permanently wingless queens; these traits imply male‐biased dispersal. However, army ant colonies are obligately nomadic and have the potential to traverse landscapes. Eciton burchellii, the most regularly nomadic army ant, is a forest interior species: colony raiding activities are limited in the absence of forest cover. To examine whether nomadism and landscape (forest clearing and elevation) affect population genetic structure in a montane E. burchellii population, we reconstructed queen and male genotypes from 25 colonies at seven polymorphic microsatellite loci. Pairwise genetic distances among individuals were compared to pairwise geographical and resistance distances using regressions with permutations, partial Mantel tests and random forests analyses. Although there was no significant spatial genetic structure in queens or males in montane forest, dispersal may be male‐biased. We found significant isolation by landscape resistance for queens based on land cover (forest clearing), but not on elevation. Summed colony emigrations over the lifetime of the queen may contribute to gene flow in this species and forest clearing impedes these movements and subsequent gene dispersal. Further forest cover removal may increasingly inhibit Eciton burchellii colony dispersal. We recommend maintaining habitat connectivity in tropical forests to promote population persistence for this keystone species.     

Insight into post-mating interactions between the sexes: relatedness suppresses productivity of singly mated female Drosophila melanogaster

Post-mating, prefertilization inbreeding avoidance (PPIA) is well established in plants but not in animals. Support for animal PPIA comes from sperm competition studies showing success of a male's gametes declining with his relatedness to the multiply mated female; however, such studies confound female-male and male-male interaction. To avoid this problem, we investigated offspring productivity of singly mated Drosophila melanogaster females using flies from four different genetic backgrounds. Our experiments established that intrapopulation crosses using highly related parents (within-strain) were significantly less productive than intrapopulation crosses using unrelated individuals from the same population (between-strain). Furthermore, we showed that these effects were not due to inbreeding depression. The average decrease in offspring productivity of within-strain crosses relative to between-strain crosses was 18.3% [nonlaboratory populations: Zimbabwe 20.3%, Riverside 11.4%, neither of which showed inbreeding depression; and temperature-adapted laboratory populations, uncorrected (corrected) for nonsignificant inbreeding depression: 18 degrees C, 26.5% (24.2%) and 29 degrees C, 20.1% (9.5%)]. The significant reduction of within-cross productivity demonstrates PPIA in the absence of multiple mating.     

Inbreeding is associated with shorter early-life telomere length in a wild passerine

Inbreeding can have negative effects on survival and reproduction, which may be of conservation concern in small and isolated populations. However, the physiological mechanisms underlying inbreeding depression are not well-known. The length of telomeres, the DNA sequences protecting chromosome ends, has been associated with health or fitness in several species. We investigated effects of inbreeding on early-life telomere length in two small island populations of wild house sparrows (Passer domesticus) known to be affected by inbreeding depression. Using genomic measures of inbreeding we found that inbred nestling house sparrows (n?=?371) have significantly shorter telomeres. Using pedigree-based estimates of inbreeding we found a tendency for inbred nestling house sparrows to have shorter telomeres (n?=?1195). This negative effect of inbreeding on telomere length may have been complemented by a heterosis effect resulting in longer telomeres in individuals that were less inbred than the population average. Furthermore, we found some evidence of stronger effects of inbreeding on telomere length in males than females. Thus, telomere length may reveal subtle costs of inbreeding in the wild and demonstrate a route by which inbreeding negatively impacts the physiological state of an organism already at early life-history stages.

     

How much gene flow is needed to avoid inbreeding depression in wild tiger populations?

The number and size of tiger populations continue to decline owing to habitat loss, habitat fragmentation and poaching of tigers and their prey. As a result, tiger populations have become small and highly structured. Current populations have been isolated since the early 1970s or for approximately seven generations. The objective of this study is to explore how inbreeding may be affecting the persistence of remaining tiger populations and how dispersal, either natural or artificial, may reduce the potentially detrimental effect of inbreeding depression. We developed a tiger simulation model and used published levels of genetic load in mammals to simulate inbreeding depression. Following a 50 year period of population isolation, we introduced one to four dispersing male tigers per generation to explore how gene flow from nearby populations may reduce the negative impact of inbreeding depression. For the smallest populations, even four dispersing male tigers per generation did not increase population viability, and the likelihood of extinction is more than 90% within 30 years. Unless habitat connectivity is restored or animals are artificially introduced in the next 70 years, medium size wild populations are also likely to go extinct, with only four to five of the largest wild tiger populations likely to remain extant in this same period without intervention. To reduce the risk of local extinction, habitat connectivity must be pursued concurrently with efforts to increase population size (e.g. enhance habitat quality, increase habitat availability). It is critical that infrastructure development, dam construction and other similar projects are planned appropriately so that they do not erode the extent or quality of habitat for these populations so that they can truly serve as future source populations.     

Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population

1. Conservation biologists are concerned about the interactive effects of environmental stress and inbreeding because such interactions could affect the dynamics and extinction risk of small and isolated populations, but few studies have tested for these interactions in nature. 2. We used data from the long-term population study of song sparrows Melospiza melodia on Mandarte Island to examine the joint effects of inbreeding and environmental stress on four fitness traits that are known to be affected by the inbreeding level of adult birds: hatching success, laying date, male mating success and fledgling survival. 3. We found that inbreeding depression interacted with environmental stress to reduce hatching success in the nests of inbred females during periods of rain. 4. For laying date, we found equivocal support for an interaction between parental inbreeding and environmental stress. In this case, however, inbred females experienced less inbreeding depression in more stressful, cooler years. 5. For two other traits, we found no evidence that the strength of inbreeding depression varied with environmental stress. First, mated males fathered fewer nests per season if inbred or if the ratio of males to females in the population was high, but inbreeding depression did not depend on sex ratio. Second, fledglings survived poorly during rainy periods and if their father was inbred, but the effects of paternal inbreeding and rain did not interact. 6. Thus, even for a single species, interactions between the inbreeding level and environmental stress may not occur in all traits affected by inbreeding depression, and interactions that do occur will not always act synergistically to further decrease fitness.     

Heterozygosity-fitness correlations among wild populations of European tree frog (Hyla arborea) detect fixation load

Quantifying the impacts of inbreeding and genetic drift on fitness traits in fragmented populations is becoming a major goal in conservation biology. Such impacts occur at different levels and involve different sets of loci. Genetic drift randomly fixes slightly deleterious alleles leading to different fixation load among populations. By contrast, inbreeding depression arises from highly deleterious alleles in segregation within a population and creates variation among individuals. A popular approach is to measure correlations between molecular variation and phenotypic performances. This approach has been mainly used at the individual level to detect inbreeding depression within populations and sometimes at the population level but without consideration about the genetic processes measured. For the first time, we used in this study a molecular approach considering both the interpopulation and intrapopulation level to discriminate the relative importance of inbreeding depression vs. fixation load in isolated and non-fragmented populations of European tree frog (Hyla arborea), complemented with interpopulational crosses. We demonstrated that the positive correlations observed between genetic heterozygosity and larval performances on merged data were mainly caused by co-variations in genetic diversity and fixation load among populations rather than by inbreeding depression and segregating deleterious alleles within populations. Such a method is highly relevant in a conservation perspective because, depending on how populations lose fitness (inbreeding vs. fixation load), specific management actions may be designed to improve the persistence of populations.     

Interpopulation variation in mating system and late-stage inbreeding depression in Magnolia stellata

Inbreeding has the potential to cause evolutionary changes in populations, although these changes are likely to drive populations to extinction through inbreeding depression and reductions in genetic diversity. We investigated the mating system and late-stage inbreeding depression (δ) in 10 populations of Magnolia stellata using nine microsatellite markers and evaluated the effects of population size and the degree of population isolation through inbreeding and inbreeding depression on the persistence of populations. The outcrossing rates were very similar (~0.7) among populations, but the correlations of paternity, fractions of biparental inbreeding and inbreeding coefficients at the seed stage ( F _S) varied among populations, suggesting that the level of outcrossing was similar among populations, while the quality of it was not. A significant negative correlation was detected between F _S and population size. The average value of δ was 0.709, and the values in six of the 10 populations were significant. The values of δ differed among populations, although clear relationships with population size and the degree of population isolation were not detected. However, in one population, which was very small and located in the edge of the species' range, we obtained a very low value of δ (–0.096), which may be indicative of purging or the fixation of deleterious alleles. Existing M. stellata populations that are small (and thus might be expected to have higher frequencies of inbreeding) and have large values of δ may be in danger of declining, even if the populations are located within the central region of the species' range.     

Persistence of the gypsophile <Emphasis Type="Italic">Lepidospartum burgessii</Emphasis> (Asteraceae) through clonal growth and limited gene flow

Lepidospartum burgessii is a rare gypsophilic shrub with limited distribution in New Mexico and Texas. Most of the known plants are restricted to two large populations, with a few small, isolated populations scattered in the surrounding area. The low recruitment observed in the two largest populations may be due to low seed set resulting from high inbreeding and/or self-incompatibility. We used eight microsatellite loci to quantify diversity, relatedness, inbreeding, population structure, and frequency of clonal reproduction. Seed collections were made to quantify seed set and germination rates. Overall, there was a moderate level of clonal diversity within patches of L. burgessii indicating asexual growth is important for population persistence. Inbreeding coefficients were high both between and within populations. Most patches showed a significant level of relatedness between individuals. At a fine scale, patches within populations were significantly different from each other, however when all patches were combined, the two populations of L. burgessii were not genetically distinct. Compared to a population of its common congener, Lepidospartum latisquamum, L. burgessii populations had similar measures of diversity, more clonal reproduction, and lower germination rates. High relatedness and inbreeding may explain the low seed set and recruitment in L. burgessii, however factors such as insect herbivory and precipitation changes may further depress recruitment.