Inbreeding and inbreeding depression of early life traits in a cooperative mammal

Mating between relatives often results in negative fitness consequences or inbreeding depression. However, the expression of inbreeding in populations of wild cooperative mammals and the effects of environmental, maternal and social factors on inbreeding depression in these systems are currently not well understood. This study uses pedigree‐based inbreeding coefficients from a long‐term study of meerkats (Suricata suricatta) in South Africa to reveal that 44% of the population have detectably non‐zero (F > 0) inbreeding coefficients. 15% of these inbred individuals were the result of moderate inbreeding (F ≥ 0.125), although such inbreeding events almost solely occurred when mating individuals had no prior experience of each other. Inbreeding depression was evident for a range of traits: pup mass at emergence from the natal burrow, hind‐foot length, growth until independence and juvenile survival. However, we found no evidence of significant inbreeding depression for skull and forearm length or for pup survival. This research provides a rare investigation into inbreeding in a cooperative mammal, revealing high levels of inbreeding, considerable negative consequences and complex interactions with the social environment.     

Mate availability contributes to maintain the mixed‐mating system in a scolytid beetle

We investigated the mating system and population genetic structure of the beetle, Coccotrypes dactyliperda, with life history characteristics that suggest the presence of a stable mixed‐mating system. We examined the genetic structure of seven populations in Israel and found significant departures from the Hardy–Weinberg equilibrium and an excess of homozygosity. Inbreeding coefficients were highly variable across populations, suggesting that low levels of outbreeding occur in nature. Experiments were conducted to determine whether the observed high inbreeding in these populations is the result of a reproductive assurance strategy. Females reared in the laboratory took longer to mate with males from the same population (inbreeding) than with males from a different population (outbreeding). These results suggest that females delayed inbreeding, and were more inclined to outbreed when possible. Thus inbreeding, which predominates in most populations, may be due to a shortage of mates for outbreeding rather than a preference for inbreeding. We conclude that C. dactyliperda has a mixed‐mating system that may be maintained by a reproductive assurance strategy.     

Inbreeding depression in Campanula rapunculoides L. I. A comparison of inbreeding depression in plants derived from strong and weak self-incompatibility phenotypes

The evolution of selfing taxa from outcrossing ancestors has occurred repeatedly and is the subject of many theoretical models, yet few empirical studies have examined the immediate consequences of inbreeding in a population with variable expression of self-incompatibility. Because self-incompatibility breaks down with floral age in Campanula rapunculoides, we were able to mate outbred and selfed maternal plants in a crossing design which produced progeny with inbreeding coefficients of 0, 0.25, 0.50 and 0.75. Cumulative inbreeding depression in plants that were selfed for one generation was very high in families derived from strongly self-incompatible plants (average δ = 0.98), and somewhat lower in families derived from plants with weaker expression of self-incompatibility (average δ = 0.90). Relative to outbred progeny, inbred progeny produced fewer seeds, had lower rates of germination, less vegetative growth and fewer flowers per plant. Inbred progeny also took longer to germinate, and longer to produce a first leaf and to flower. Interestingly, inbred plants also produced 40% fewer seeds than outcrossed plants (t-test P < 0.001) even when mated to the same, unrelated pollen donor, suggesting that inbreeding can produce profound maternal effects. Most importantly, our results demonstrate that progeny derived from plants with stronger expression of self-incompatibility exhibited greater levels of inbreeding depression than progeny from plants with weaker expression of self-incompatibility. Moreover, the decline in fitness (cumulative, ln-transformed) over the four inbreeding levels was steeper for the progeny of the strongly self-incompatible lineages. These empirical results suggest that inbreeding depression and mating system phenotype have the potential to coevolve.     

Inbreeding and inbreeding depression in endangered red wolves (Canis rufus)

In natural populations, the expression and severity of inbreeding depression can vary widely across taxa. Describing processes that influence the extent of inbreeding and inbreeding depression aid in our understanding of the evolutionary history of mating systems such as cooperative breeding and nonrandom mate selection. Such findings also help shape wildlife conservation theory because inbreeding depression reduces the viability of small populations. We evaluated the extent of inbreeding and inbreeding depression in a small, re‐introduced population of red wolves (Canis rufus) in North Carolina. Since red wolves were first re‐introduced in 1987, pedigree inbreeding coefficients (f) increased considerably and almost every wild born wolf was inbred (average f = 0.154 and max f = 0.383). The large inbreeding coefficients were due to both background relatedness associated with few founders and numerous close relative matings. Inbreeding depression was most evident for adult body size and generally absent for direct fitness measures such as reproductive success and survival; no lethal equivalents (LE = 0.00) were detected in juvenile survival. The lack of strong inbreeding depression in direct measures of fitness could be due to a founder effect or because there were no outbred individuals for comparison. Our results highlight the variable expression of inbreeding depression across traits and the need to measure a number of different traits when evaluating inbreeding depression in a wild population.     

Apparent inbreeding preference despite inbreeding depression in the American crow

Although matings between relatives can have negative effects on offspring fitness, apparent inbreeding preference has been reported in a growing number of systems, including those with documented inbreeding depression. Here, we examined evidence for inbreeding depression and inbreeding preference in two populations (Clinton, New York, and Davis, California, USA) of the cooperatively breeding American crow (Corvus brachyrhynchos). We then compared observed inbreeding strategies with theoretical expectations for optimal, adaptive levels of inbreeding, given the inclusive fitness benefits and population‐specific magnitude of inbreeding depression. We found that low heterozygosity at a panel of 33 microsatellite markers was associated with low survival probability (fledging success) and low white blood cell counts among offspring in both populations. Despite these costs, our data were more consistent with inbreeding preference than avoidance: The observed heterozygosity among 396 sampled crow offspring was significantly lower than expected if local adults were mating by random chance. This pattern was consistent across a range of spatial scales in both populations. Adaptive levels of inbreeding, given the magnitude of inbreeding depression, were predicted to be very low in the California population, whereas complete disassortative mating was predicted in the New York population. Sexual conflict might have contributed to the apparent absence of inbreeding avoidance in crows. These data add to an increasing number of examples of an “inbreeding paradox,” where inbreeding appears to be preferred despite inbreeding depression.     

Inbreeding and extinction: Effects of rate of inbreeding

Deleterious alleles may be removed (purged) bynatural selection in populations undergoinginbreeding. However, there is controversyregarding the effectiveness of selection inreducing the risk of extinction due toinbreeding, especially in relation to the rateof inbreeding. We evaluated the effect of therate of inbreeding on reducing extinction risk,in populations of Drosophila melanogastermaintained using full-sib mating (160replicates), or at effective population sizes(N _e) of 10 (80) or 20 (80).Extinction rates in the populations maintainedusing full-sib mating occurred at lower levelsof inbreeding than in the larger populations,whereas the two larger populations did notdiffer significantly from each other.Inbreeding coefficients at 50% extinction were0.62, 0.79 and 0.77 for the full-sib (N _e = 2.6), N _e = 10 and N _e = 20 treatments, respectively. Populations of N _e = 20 that remained extant after 60 generations, showed inbreeding depression, with the mean fitness of these populations being only 45% of the outbredcontrols. There was considerable variationamong the 31 inbred populations in fitness, butnone of the N _e = 20 populations hadfitness that was higher than the outbredcontrol. We conclude that purging may slow therate of extinction slightly, but it cannot berelied on to eliminate the deleterious effectsof inbreeding.     

THE RELATIONSHIP BETWEEN INBREEDING DEPRESSION AND PRIOR INBREEDING AMONG POPULATIONS OF FOUR MIMULUS TAXA

When recessive mutations are the primary cause of inbreeding depression, a negative relationship between the levels of prior inbreeding and inbreeding depression is expected. We tested this prediction using 15 populations chosen a priori to represent a wide range of prior inbreeding among four closely related taxa of the Mimulus guttatus species complex. Artificially selfed and outcrossed progeny were grown under controlled growth-chamber conditions, and inbreeding depression was estimated for each population as one minus the ratio of the fitness of selfed to outcrossed progeny. Estimates of inbreeding depression varied from 0% to 68% among populations. Inbreeding coefficients, estimated from electrophoretic assay of field-collected progenies, ranged from 0.02 to 0.76. All five fitness traits displayed a negative association between inbreeding depression and the inbreeding coefficient, but only height showed a statistically significant correlation. Inbreeding depression was also not correlated with the level of genetic variability. In addition, populations with similar levels of prior inbreeding showed significant differences of inbreeding depression, whereas populations with different levels of prior inbreeding showed similar inbreeding depression. Within populations, inbreeding depression did not differ between progeny selfed one versus two generations. Our results are weakly consistent with the recessive mutation model of inbreeding depression, but suggest that additional factors, including genotype-by-environment interaction and complex modes of inheritance, may influence the expression of inbreeding depression.     

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.     

Genetic diversity and seed production in Santa Lucia fir (Abies bracteata), a relict of the Miocene Broadleaved Evergreen Forest

Santa Lucia fir (Abies bracteata), is a unique fir, the sole member of the subgenus Pseudotorreya. It is a relict of the Miocene broadleaved evergreen sclerophyll forest, and is now restricted to a highly fragmented range in the Santa Lucia Mountains of central coastal California. Expected heterozygosity for 30 isozyme loci in 18 enzyme systems, averaged over six populations that spanned the species’ north–south range, was only 0.036. Despite a fragmented range and isolated populations, differentiation (F _ST) was only 0.080 for mature trees, and the number of migrants per generation (Nm) was 2.88 or 3.83, depending on the method of estimation. F _ST for embryos was lower, 0.025, and Nm correspondingly higher, 9.75. Nei’s genetic distances were small and unrelated to geographic distances between populations. The proportion of full seeds per cone was only 0.082–0.488, depending on population, which suggests a high incidence of selfing followed by embryo abortion. However, the level of accumulated inbreeding, F _IS, in mature trees was low, only 0.049. By contrast, F _IS for embryos was 0.388, which indicates a high proportion of selfed progeny, in agreement with the low seed yields. The difference in inbreeding coefficients between seed trees and their progeny suggest that most inbreds are eliminated before maturity and, therefore, seed production, already low, overestimates the true potential for regeneration of these populations. These results have implications for conservation.     

Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: do hermaphrodites need males for complete fertilization?

Androdioecy (populations comprised of mixtures of males and hermaphrodites) is a rare mating system, found only in a few plants and animals. The rarity of this system stems from the limited benefits to males in an otherwise all-hermaphroditic population. One of the potential benefits to males is typified by the nematode Caenorhabditis elegans, in which hermaphrodites do not produce sufficient sperm to fertilize all of their eggs. Here we explore the possibility that males are needed for complete fertilization of hermaphrodites' eggs in a second androdioecious animal, the clam shrimp Eulimnadia texana. We compare the fertilization rate of outcrossed to selfed eggs to test whether the latter exhibit lower fertilization due to sperm limitation (as in C. elegans). Because this comparison confounds differences in egg fertilization due to sperm limitation with the potential for early inbreeding depression, we also used a third mating treatment, a brother/sister cross, to allow separation of sperm limitation from inbreeding depression. In both populations examined, the proportion of eggs that were fertilized decreased linearly with increasing relatedness: comparing eggs produced by outcrossing, brother/sister, and selfed matings, respectively. This pattern suggests that differences in fertilization among these three treatments were caused solely by inbreeding depression, and therefore that hermaphrodites are not sperm limited. These results are combined with previous data on this species to test whether the maintenance of males can be explained using a population genetics model specifically designed for this species.     

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.     

Genetic diversity,sexual condition,and microhabitat preference determine mating patterns in Sphagnum (Sphagnaceae) peat‐mosses

In bryophytes, the possibility of intragametophytic selfing creates complex mating patterns that are not possible in seed plants, although relatively little is known about patterns of inbreeding in natural populations. In the peat‐moss genus Sphagnum, taxa are generally bisexual (gametophytes produce both sperm and egg) or unisexual (gametes produced by separate male and female plants). We sampled populations of 14 species, aiming to assess inbreeding variation and inbreeding depression in sporophytes, and to evaluate correlations between sexual expression, mating systems, and microhabitat preferences. We sampled maternal gametophytes and their attached sporophytes at 12–19 microsatellite loci. Bisexual species exhibited higher levels of inbreeding than unisexual species but did generally engage in some outcrossing. Inbreeding depression did not appear to be common in either unisexual or bisexual species. Genetic diversity was higher in populations of unisexual species compared to populations of bisexual species. We found a significant association between species microhabitat preference and population genetic diversity: species preferring hummocks (high above water table) had populations with lower diversity than species inhabiting hollows (at the water table). We also found a significant interaction between sexual condition, microhabitat preference, and inbreeding coefficients, suggesting a vital role for species ecology in determining mating patterns in Sphagnum populations. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 96–113.     

Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population

Inbreeding is common in small and threatened populations and often has a negative effect on individual fitness and genetic diversity. Thus, inbreeding can be an important factor affecting the persistence of small populations. In this study, we investigated the effects of inbreeding on fitness in a small, wild population of house sparrows (Passer domesticus) on the island of Aldra, Norway. The population was founded in 1998 by four individuals (one female and three males). After the founder event, the adult population rapidly increased to about 30 individuals in 2001. At the same time, the mean inbreeding coefficient among adults increased from 0 to 0.04 by 2001 and thereafter fluctuated between 0.06 and 0.10, indicating a highly inbred population. We found a negative effect of inbreeding on lifetime reproductive success, which seemed to be mainly due to an effect of inbreeding on annual reproductive success. This resulted in selection against inbred females. However, the negative effect of inbreeding was less strong in males, suggesting that selection against inbred individuals is at least partly sex specific. To examine whether individuals avoided breeding with close relatives, we compared observed inbreeding and kinship coefficients in the population with those obtained from simulations of random mating. We found no significant differences between the two, indicating weak or absent inbreeding avoidance. We conclude that there was inbreeding depression in our population. Despite this, birds did not seem to actively avoid mating with close relatives, perhaps as a consequence of constraints on mating possibilities in such a small population.     

INBREEDING AND VARIANCE EFFECTIVE SIZES FOR NONRANDOM MATING POPULATIONS

Following an inbreeding approach and assuming discrete generations and autosomal inheritance involving genes that do not affect viability or reproductive ability, I have derived expressions for the inbreeding effective size, N_eI, for a finite diploid population with variable census sizes for three cases: monoecious populations with partial selfing; dioecious populations of equal numbers of males and females with partial sib mating; and unequal numbers of males and females with random mating. For the first two cases, recurrence equations for the inbreeding coefficient are also obtained, which allow inbreeding coefficients to be predicted exactly in both early and late generations. Following the variance of change in gene frequency approach, a general expression for variance effective size, N_eV, is obtained for a population with unequal numbers of male and female individuals, arbitrary family size distribution, and nonrandom mating. All the parameters involved are allowed to change over generations. For some special cases, the equation reduces to the simple expressions approximately as derived by previous authors. Comparisons are made between equations derived by the present study and those obtained by previous authors. Some of the published equations for N_eI and N_eV are shown to be incomplete or incorrect. Stochastic simulations are run to check the results where disagreements with others are involved.     

Long-term progression of inbreeding depression in a Mediterranean ornithophilous shrub

The ornithophilous species Anagyris foetida L. is a Mediterranean shrub with highly fragmented populations and a mixed mating system. In a previous study, we analyzed the first 3 years of the life cycle of two progenies (selfed and outcrossed) grown from seed obtained by hand pollination and planted in an experimental garden in 2005. In that study, we found that inbreeding depression (ID) was manifested both reproductively and vegetatively throughout the life cycle, with male reproductive function being the most affected trait. In the present study, our main aim was to check the progression of the two progenies 12 years after transplantation. For this we analyzed their survival and their vegetative and reproductive traits. According to our results, levels of ID were similar to those obtained in the previous study, with some factors decreased and thus varying with the age of the studied individuals. Vegetative parameters were found to have a greater influence than reproductive ones (δ = 0.56 vs. δ = 0.36) on overall ID. As indicated by the global ID (δ = 0.72) the populations have a mating system that is intermediate between outcrossing and a mixed system. Furthermore, the lower male reproductive capacity of the selfed individuals has been maintained over time. Our study also demonstrates the importance of studying the ID value throughout the life cycle of plants.     

IMMUNOCHEMICAL COMPARISONS OF SEED PROTEINS FROM POPULATIONS OF PINUS RADIATA (PINACEAE)

Antisera were prepared to seed proteins from five populations of Pinus radiata and to seed proteins from six other pine species. Differences between the P. radiata populations detected with these antisera were compared to differences in sizes of cones from the same populations. The strong correlation between antigenic differences and cone size differences provides evidence that in P. radiata, both seed proteins and cone size indicate quantitative genetic relationships among the populations. The data suggest that the three California mainland populations of P. radiata are more closely related to one another than to the insular populations, and that the insular populations are more closely related to each other than to the California populations, to P. attenuata, or to P. muricata.     

Reduced mate availability leads to evolution of self‐fertilization and purging of inbreeding depression in a hermaphrodite

Basic models of mating‐system evolution predict that hermaphroditic organisms should mostly either cross‐fertilize, or self‐fertilize, due to self‐reinforcing coevolution of inbreeding depression and outcrossing rates. However transitions between mating systems occur. A plausible scenario for such transitions assumes that a decrease in pollinator or mate availability temporarily constrains outcrossing populations to self‐fertilize as a reproductive assurance strategy. This should trigger a purge of inbreeding depression, which in turn encourages individuals to self‐fertilize more often and finally to reduce male allocation. We tested the predictions of this scenario using the freshwater snail Physa acuta, a self‐compatible hermaphrodite that preferentially outcrosses and exhibits high inbreeding depression in natural populations. From an outbred population, we built two types of experimental evolution lines, controls (outcrossing every generation) and constrained lines (in which mates were often unavailable, forcing individuals to self‐fertilize). After ca. 20 generations, individuals from constrained lines initiated self‐fertilization earlier in life and had purged most of their inbreeding depression compared to controls. However, their male allocation remained unchanged. Our study suggests that the mating system can rapidly evolve as a response to reduced mating opportunities, supporting the reproductive assurance scenario of transitions from outcrossing to selfing.     

Inbreeding avoidance and the evolution of gender dimorphism in Wurmbea biglandulosa (Colchicaceae)

How females establish in populations of cosexuals is central to understanding the evolution of gender dimorphism in angiosperms. Inbreeding avoidance hypotheses propose that females can establish and be maintained if cosexual fitness is reduced because they self-fertilize, and their progeny express inbreeding depression. Here we assess the role of inbreeding avoidance in maintaining sexual system variation in Wurmbea biglandulosa. We estimated costs of self-pollination, mating patterns, and inbreeding depression in gender monomorphic (cosexuals only) and dimorphic (males and females) populations. Costs of selfing, estimated from seed set of experimentally self- and cross-pollinated flowers, were severe in both males and cosexuals (inbreeding depression, sigma = 0.86). In a field experiment, intact males that could self produced fewer seeds than both emasculated males and females, whereas seed set of intact and emasculated cosexuals did not differ. Thus, pollinator-mediated selfing reduces fitness of males but not cosexuals under natural conditions. Outcrossing rates of males revealed substantial selfing (t = 0.68), whereas females and cosexuals were outcrossed (0.92 and 0.97). For males, progeny inbreeding coefficients exceeded parental coefficients (0.220 vs. 0.009), whereas for females and cosexuals these coefficients did not differ and approached zero. Differences in coefficients between males and their progeny indicate that selfed progeny express severe inbreeding depression (sigma = 0.93). Combined with inbreeding depression for seed set, cumulative sigma = 0.99, indicating that most or all selfed zygotes fail to reach reproductive maturity. We propose that present sexual system variation in W. biglandulosa is maintained by high inbreeding depression coupled with differences in selfing rates among monomorphic and dimorphic populations.     

THE ROLE OF GENES OF LARGE EFFECT ON INBREEDING DEPRESSION IN MIMULUS GUTTATUS

Severe inbreeding depression is routinely observed in outcrossing species. If inbreeding load is due largely to deleterious alleles of large effect, such as recessive lethals or steriles, then most of it is expected to be purged during brief periods of inbreeding. In contrast, if inbreeding depression is due to the cumulative effects of many deleterious alleles of small effect, then it will be maintained in the face of periodic inbreeding. Whether or not inbreeding depression can be purged with inbreeding in the short term has important implications for the evolution of mating systems and the probability that a small population will go extinct. In this paper I evaluate the extent to which the tremendous inbreeding load in a primarily outcrossing population of the wildflower, Mimulus guttatus, is due to alleles of large effect. To do this, I first constructed a large outbred “ancestral” population by randomly mating plants collected as seeds from a natural population. From this population I formed 1200 lines that were maintained by self-fertilization and single seedling descent: after five generations of selling, 335 lines had survived the inbreeding process. Selection during the line formation is expected to have largely purged alleles of large effect from the collection of highly inbred lines. Because alleles with minor effects on fitness should have been effectively neutral, the inbreeding depression due to this class of genes should have been unchanged. The inbred lines were intercrossed to form a large, outcrossed “purged” population. Finally, I estimated the fitness of outbred and selfed progeny from the ancestral and purged populations to determine the contribution of major deleterious alleles on inbreeding depression. I found that although the average fitness of the outcrossed progeny nearly doubled following purging, the limited decline in inbreeding depression and limited increase in inbred fitness indicates that alleles of large effect are not the principle cause of inbreeding depression in this population. In aggregate, the data suggest that lethals and steriles make a minority contribution to inbreeding depression and that the increased outbred fitness is due primarily to adaptation to greenhouse conditions.     

Limiting inbreeding in disjunct and isolated populations of a woody shrub

Pollen movements and mating patterns are key features that influence population genetic structure. When gene flow is low, small populations are prone to increased genetic drift and inbreeding, but naturally disjunct species may have features that reduce inbreeding and contribute to their persistence despite genetic isolation. Using microsatellite loci, we investigated outcrossing levels, family mating parameters, pollen dispersal, and spatial genetic structure in three populations of Hakea oldfieldii, a fire‐sensitive shrub with naturally disjunct, isolated populations prone to reduction in size and extinction following fires. We mapped and genotyped a sample of 102 plants from a large population, and all plants from two smaller populations (28 and 20 individuals), and genotyped 158–210 progeny from each population. We found high outcrossing despite the possibility of geitonogamous pollination, small amounts of biparental inbreeding, a limited number of successful pollen parents within populations, and significant correlated paternity. The number of pollen parents for each seed parent was moderate. There was low but significant spatial genetic structure up to 10 m around plants, but the majority of successful pollen came from outside this area including substantial proportions from distant plants within populations. Seed production varied among seven populations investigated but was not correlated with census population size. We suggest there may be a mechanism to prevent self‐pollination in H. oldfieldii and that high outcrossing and pollen dispersal within populations would promote genetic diversity among the relatively small amount of seed stored in the canopy. These features of the mating system would contribute to the persistence of genetically isolated populations prone to fluctuations in size.