Genetic diversity and mating system of the threatened plant <Emphasis Type="Italic">Kirengeshoma palmata</Emphasis> (Saxifragaceae) in Korea

The endangered herb Kirengeshoma palmata, from eastern Asia, has had its population severely reduced in number through habitat loss and fragmentation. All of the individuals within five subgroups at Mt. Baek-un-san, in the southern part of Korea, were genetically surveyed by allozyme analysis. Genetic diversity levels within subgroups were relatively high, and a consistently high outcrossing rate as well as a negligible biparental mating rate were confirmed by this study. Several groups of visibly connected ramets were observed in a clustered distribution which suggested cloning. Absence of mating partner rather than pollinators decreased seed production in small mating groups. The present genetic structure of the five subgroups was probably the result of local extinction of intervening populations. Because K. palmata may be a self-incompatible species, populations with few genets face lowered seed set due to mate scarcity. Thus, this type of population may be at an increased risk of extinction as a result of inbreeding depression, loss of genetic variability, and reduced sexual reproduction. The small, genetically depauperate subgroups may need an input of seeds or plants from other populations in China or Japan in order to regenerate, but the possibility of outcrossing depression leads us to recommend outbreeding among the local subgroups of Mt. Baek-un-san to restore genetic variability.     

Evolutionarily stable mixed mating in a variety of genetic systems

Many species display a mixture of close inbreeding and outbreeding which is referred to as mixed mating. For selfing species, models predict that such mixed mating systems can be stable. Conversely, models considering separate sex species have not been able to explain mixed mating systems. This failure may be a result of the unrealistic assumption that recurrent inbreeding does not increase the inbreeding coefficient. Here we show that mixed mating is expected in separate sex systems when recurrent inbreeding is taken into account. A female that allows her brother to sibmate with her gives an extra mating opportunity to said brother. This kin selective advantage should be strongest in genetic systems where the male is more related to the female. In support of this idea, we find that inbreeding evolves most easily in selfers, followed by diploid sibmating, followed by haplodiploid sibmating. Consideration of published values for the regression of fitness on inbreeding coefficient suggests that many species fall in a range where some selfing/sibmating is optimal.     

THE EVOLUTION OF ASSORTATIVE MATING AND SELFING WITH IN- AND OUTBREEDING DEPRESSION

The effect of inbreeding and outbreeding depression on the evolution of assortment are often considered separately. For instance, inbreeding depression is usually thought to shape selfing rates whereas outbreeding depression is commonly thought to affect the evolution of assortative mating. In this article, we consider the evolution of assortment in a context of local adaptation and we show that it is a typical situation in which both effects act simultaneously to shape the degree of selfing or assortative mating. More specifically, we show that selection on a modifier of mating can be partitioned into three distinct effects: a transmission advantage, an association to heterozygosity (proportional to inbreeding depression), and an association to beneficial alleles (proportional to outbreeding depression), so that random mating may evolve even with strong local adaptation. In addition, we show that it is necessary to carefully delimit the conditions for polymorphism at local adaptation locus to study the evolution of assortment. In particular, the range of parameters most favorable to the maintenance of polymorphism corresponds to situations favoring less assortment.     

Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata

Empirical studies in vertebrates support the hypothesis that inbreeding reduces resistance against parasites and pathogens. However, studies in insects have not found any evidence that inbreeding compromises immune defence. Here we tested whether one generation of brother-sister mating or extreme outbreeding (mating between two populations) have an effect on innate immunity and life history traits in the autumnal moth, Epirrita autumnata. We show that the effect of inbreeding on immune response differed between the sexes: whereas in females, inbreeding significantly reduced encapsulation response against nylon monofilament ability, it did not have a significant effect on male immune response. There were also differences in the correlation of the immune response with other traits: in females increased immune response was positively correlated with large size, whereas in males immune response increased with a reduction in development time. Immune response differed significantly among families in males but not in females, both for the inbreeding and extreme outbreeding experiments. In conjunction with the observed immune responses to inbreeding, these data suggest that in males genetic variation for immune response is largely additive or non-directional with respect to dominance, whereas in females variation is much reduced and consists of directional dominance variance. Further, we show that encapsulation response against nylon monofilament is associated with the resistance against real pathogens suggesting that this widely used method to measure the strength of immune defence in insects is also a biologically relevant method.     

Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management

As populations become increasingly fragmented, managers are often faced with the dilemma that intentional hybridization might save a population from inbreeding depression but it might also induce outbreeding depression. While empirical evidence for inbreeding depression is vastly greater than that for outbreeding depression, the available data suggest that risks of outbreeding, particularly in the second generation, are on par with the risks of inbreeding. Predicting the relative risks in any particular situation is complicated by variation among taxa, characters being measured, level of divergence between hybridizing populations, mating history, environmental conditions and the potential for inbreeding and outbreeding effects to be occurring simultaneously. Further work on consequences of interpopulation hybridization is sorely needed with particular emphasis on the taxonomic scope, the duration of fitness problems and the joint effects of inbreeding and outbreeding. Meanwhile, managers can minimize the risks of both inbreeding and outbreeding by using intentional hybridization only for populations clearly suffering from inbreeding depression, maximizing the genetic and adaptive similarity between populations, and testing the effects of hybridization for at least two generations whenever possible.     

OUTBREEDING DEPRESSION WITH LOW GENETIC VARIATION IN SELFING CAENORHABDITIS NEMATODES

Theory and empirical study produce clear links between mating system evolution and inbreeding depression. The connections between mating systems and outbreeding depression, whereby fitness is reduced in crosses of less related individuals, however, are less well defined. Here we investigate inbreeding and outbreeding depression in self‐fertile androdioecious nematodes, focusing on Caenorhabditis sp. 11. We quantify nucleotide polymorphism for nine nuclear loci for strains throughout its tropical range, and find some evidence of genetic differentiation despite the lowest sequence diversity observed in this genus. Controlled crosses between strains from geographically separated regions show strong outbreeding depression, with reproductive output of F1s reduced by 36% on average. Outbreeding depression is therefore common in self‐fertilizing Caenorhabditis species, each of which evolved androdioecious selfing hermaphroditism independently, but appears strongest in C. sp. 11. Moreover, the poor mating efficiency of androdioecious males extends to C. sp. 11. We propose that self‐fertilization is a key driver of outbreeding depression, but that it need not evolve as a direct result of local adaptation per se. Our verbal model of this process highlights the need for formal theory, and C. sp. 11 provides a convenient system for testing the genetic mechanisms that cause outbreeding depression, negative epistasis, and incipient speciation.     

INBREEDING AS A STRATEGY IN SUBDIVIDED POPULATIONS

A generalized expression for coefficients of consanguinity and relationship with previous inbreeding is presented to examine various breeding strategies in subdivided populations. Conditions that would favor inbreeding are developed for: 1) nonfamilial inbreeding within a deme versus outbreeding; 2) altruistic inbreeding by females versus outbreeding; 3) sib-mating versus outbreeding; and 4) sib-mating versus nonfamilial breeding within a deme. Inbreeding behavior is advantageous under certain conditions but depends on the types of mating, the previous breeding history of the deme, the rate of accumulation of inbreeding depression, and the cost of migration. In polygynous mating systems it is genetically more advantageous for males to migrate, because female emigration may 1) leave a related male with no mate or one fewer mate, or 2) force both male and female to risk the cost of migration. Nonfamilial breeding is always a better strategy than sib-mating given previous inbreeding within the deme. Even when the cost of migration is zero, inbreeding is favored if the coefficient of relationship among relatives is greater than the ratio of the probabilities of offspring inviability to offspring viability. Although high inbreeding coefficients are probably not adaptive unless the costs of migration are great or inbreeding depression constants are small, low levels of inbreeding are advantageous in many situations. Therefore, increased genetic representation by way of inbreeding and inclusive fitness is a major component of the evolutionary process.     

Inbreeding avoidance in spiders: evidence for rescue effect in fecundity of female spiders with outbreeding opportunity

Selection by inbreeding depression should favour mating biases that reduce the risk of fertilization by related mates. However, equivocal evidence for inbreeding avoidance questions the strength of inbreeding depression as a selective force in the evolution of mating biases. Lack of inbreeding avoidance can be because of low risk of inbreeding, variation in tolerance to inbreeding or high costs of outbreeding. We examined the relationship between inbreeding depression and inbreeding avoidance adaptations under two levels of inbreeding in the spider Oedothorax apicatus, asking whether preference for unrelated sperm via pre- and/or post-copulatory mechanisms could restore female fitness when inbreeding depression increases. Using inbred isofemale lines we provided female spiders with one or two male spiders of different relatedness in five combinations: one male sib; one male nonsib; two male sibs; two male nonsibs; one male sib and one male nonsib. We assessed the effect of mating treatment on fecundity and hatching success of eggs after one and three generations of inbreeding. Inbreeding depression in F1 was not sufficient to detect inbreeding avoidance. In F3, inbreeding depression caused a major decline in fecundity and hatching rates of eggs. This effect was mitigated by complete recovery in fecundity in the sib-nonsib treatment, whereas no rescue effect was detected in the hatching success of eggs. The rescue effect is best explained by post-mating discrimination against kin via differential allocation of resources. The natural history of O. apicatus suggests that the costs of outbreeding may be low which combined with high costs of inbreeding should select for avoidance mechanisms. Direct benefits of post-mating inbreeding avoidance and possibly low costs of female multiple mating can favour polyandry as an inbreeding avoidance mechanism.     

Breaking taboos in the tropics: incest promotes colonization by wood-boring beetles

• 1 Inbreeding and parthenogenesis are especially frequent in colonizing species of plants and animals, and inbreeding in wood‐boring species in the weevil families Scolytinae and Platypodidae is especially common on small islands. In order to study the relationship between colonization success, island attributes and mating system in these beetles, we analysed the relative proportions of inbreeders and outbreeders for 45 Pacific and Old World tropical islands plus two adjacent mainland sites, and scored islands for size, distance from nearest source population, and maximum altitude.
• 2 The numbers of wood‐borer species decreased with decreasing island size, as expected; the degree of isolation and maximum island altitude had negligible effects on total species numbers.
• 3 Numbers of outbreeding species decreased more rapidly with island size than did those of inbreeders. Comparing species with similar ecology (e.g. ambrosia beetles) showed that this difference was best explained by differential success in colonization, rather than by differences in resource utilization or sampling biases. This conclusion was further supported by analyses of data from small islands, which suggested that outbreeding species have a higher degree of endemism and that inbreeding species are generally more widespread.
• 4 Recently established small populations necessarily go through a period of severe inbreeding, which should affect inbreeding species much less than outbreeding ones. In addition, non‐genetic ecological and behavioural (‘Allee’) effects are also expected to reduce the success of outbreeding colonists much more than that of inbreeders: compared with inbreeders, outbreeders are expected to have slower growth rates, have greater difficulties with mate‐location and be vulnerable to random extinction over a longer period.

     

Inbreeding variability and population structure in the invasive haplodiploid palm‐seed borer (Coccotrypes dactyliperda)

We investigated the mating system and population genetic structure of the invasive haplodiploid palm‐seed borer Coccotrypes dactyliperda in California. We focused on whether these primarily inbreeding beetles have a ‘mixed‐breeding’ system that includes occasional outbreeding, and whether local inbreeding coefficients (F_IS) varied with dominant environmental factors. We also analysed the genetic structure of C. dactyliperda populations across local and regional scales. Based on the analysis of genetic variation at seven microsatellite loci in 1034 individual beetles from 59 populations, we found both high rates of inbreeding and plentiful evidence of mixed‐breeding. F_IS ranged from ?0.56 to 0.90, the highest variability reported within any animal species. There was a negative correlation between F_IS and latitude, suggesting that some latitude‐associated factor affecting mating decisions influenced inbreeding rates. Multiple regressions suggested that precipitation, but not temperature, may be an important correlate. Finally, we found highly significant genetic differentiation among sites, even over short geographic distances (< 1000 m).     

The different sources of variation in inbreeding depression, heterosis and outbreeding depression in a metapopulation of Physa acuta

Understanding how parental distance affects offspring fitness, i.e., the effects of inbreeding and outbreeding in natural populations, is a major goal in evolutionary biology. While inbreeding is often associated with fitness reduction (inbreeding depression), interpopulation outcrossing may have either positive (heterosis) or negative (outbreeding depression) effects. Within a metapopulation, all phenomena may occur with various intensities depending on the focal population (especially its effective size) and the trait studied. However, little is known about interpopulation variation at this scale. We here examine variation in inbreeding depression, heterosis, and outbreeding depression on life-history traits across a full-life cycle, within a metapopulation of the hermaphroditic snail Physa acuta. We show that all three phenomena can co-occur at this scale, although they are not always expressed on the same traits. A large variation in inbreeding depression, heterosis, and outbreeding depression is observed among local populations. We provide evidence that, as expected from theory, small and isolated populations enjoy higher heterosis upon outcrossing than do large, open populations. These results emphasize the need for an integrated theory accounting for the effects of both deleterious mutations and genetic incompatibilities within metapopulations and to take into account the variability of the focal population to understand the genetic consequences of inbreeding and outbreeding at this scale.     

Outbreeding depression and breeding system evolution in small,remnant populations of <Emphasis Type="Italic">Primula vulgaris</Emphasis>: consequences for genetic rescue

Many species suffer from anthropogenic habitat fragmentation. The resulting small and isolated populations are more prone to extinction due to, amongst others, genetic erosion, inbreeding depression and Allee-effects. Genetic rescue can help mitigate such problems, but might result in outbreeding depression. We evaluated offspring fitness after selfing and outcrossing within and among three very small and isolated remnant populations of the heterostylous plant Primula vulgaris. We used greenhouse-grown offspring from these populations to test several fitness components. One population was fixed for the pin-morph, and was outcrossed with another population in the field to obtain seeds. Genetic diversity of parent and offspring populations was studied using microsatellites. Morph and population-specific heterosis, inbreeding and outbreeding depression were observed for fruit and seed set, seed weight and cumulative fitness. Highest fitness was observed in the field-outcrossed F1-population, which also showed outbreeding depression following subsequent between-population (back)crossing. Despite outbreeding depression, fitness was still relatively high. Inbreeding coefficients indicated that the offspring were more inbred than their parent populations. Offspring heterozygosity and inbreeding coefficients correlated with observed fitness. One population is evolving homostyly, showing a thrum morph with an elongated style and high autonomous fruit and seed set. This has important implications for conservation strategies such as genetic rescue, as the mating system will be altered by the introduction of homostyles.     

Outbreeding depression, but no inbreeding depression in haplodiploid Ambrosia beetles with regular sibling mating

In sexual reproduction the genetic similarity or dissimilarity between mates strongly affects offspring fitness. When mating partners are too closely related, increased homozygosity generally causes inbreeding depression, whereas crossing between too distantly related individuals may disrupt local adaptations or coadaptations within the genome and result in outbreeding depression. The optimal degree of inbreeding or outbreeding depends on population structure. A long history of inbreeding is expected to reduce inbreeding depression due to purging of deleterious alleles, and to promote outbreeding depression because of increased genetic variation between lineages. Ambrosia beetles (Xyleborini) are bark beetles with haplodiploid sex determination, strong local mate competition due to regular sibling mating within the natal chamber, and heavily biased sex ratios. We experimentally mated females of Xylosandrus germanus to brothers and unrelated males and measured offspring fitness. Inbred matings did not produce offspring with reduced fitness in any of the examined life-history traits. In contrast, outcrossed offspring suffered from reduced hatching rates. Reduction in inbreeding depression is usually attributed to purging of deleterious alleles, and the absence of inbreeding depression in X. germanus may represent the highest degree of purging of all examined species so far. Outbreeding depression within the same population has previously only been reported from plants. The causes and consequences of our findings are discussed with respect to mating strategies, sex ratios, and speciation in this unusual system.     

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.     

Quantitative genetics in conservation biology

Most of the major genetic concerns in conservation biology, including inbreeding depression, loss of evolutionary potential, genetic adaptation to captivity and outbreeding depression, involve quantitative genetics. Small population size leads to inbreeding and loss of genetic diversity and so increases extinction risk. Captive populations of endangered species are managed to maximize the retention of genetic diversity by minimizing kinship, with subsidiary efforts to minimize inbreeding. There is growing evidence that genetic adaptation to captivity is a major issue in the genetic management of captive populations of endangered species as it reduces reproductive fitness when captive populations are reintroduced into the wild. This problem is not currently addressed, but it can be alleviated by deliberately fragmenting captive populations, with occasional exchange of immigrants to avoid excessive inbreeding. The extent and importance of outbreeding depression is a matter of controversy. Currently, an extremely cautious approach is taken to mixing populations. However, this cannot continue if fragmented populations are to be adequately managed to minimize extinctions. Most genetic management recommendations for endangered species arise directly, or indirectly, from quantitative genetic considerations.     

The fitness effects of outcrossing in Calylophus serrulatus, a permanent translocation heterozygote

Small and relatively isolated populations that occupy fragmented habitat are at risk of local extinction. However, fitness consequences of fragmentation related to mating distance, such as inbreeding depression following increased self- and near-neighbor mating, may not follow standard expectations in species with specialized genetic systems. We investigated the effect of mating distance on progeny fitness in Calylophus serrulatus, a primarily autogamous, permanent translocation heterozygote that is restricted to prairie fragments in the North American tallgrass prairie region. We pollinated flowers by hand in the field with pollen sampled at various distances from the maternal parent within and between three populations in southeastern Minnesota. We raised the progeny in a greenhouse and measured fitness-related characters. Because their genetic system prevents loss of heterozygosity throughout much of the genome, regardless of inbreeding, permanent translocation heterozygotes are not expected to exhibit inbreeding depression. Consistent with this expectation, in no case did progeny of self matings suffer significantly reduced mean fitness compared to progeny from crosses between plants. Crosses between plants in the two closely situated (2 km) populations yielded progeny with fitness intermediate to their parents, but crosses between each of those populations and the more distant (20 km) population yielded progeny with reduced fitness, suggesting outbreeding depression at this largest spatial scale. Similarly, fitness of self-pollinated progeny and progeny from "near" crosses (<2 m) within populations tended to be higher than "mid" (10-25 m) and "far" (>35 m) cross-progeny fitness. Under the current conditions of fragmentation, it seems likely that the distant matings that produce outbreeding depression are rare. It appears that mean fitness in this species is maintained in the context of severe fragmentation of its populations, largely because of its genetic system.     

Genetic systems of six species ofPlantago (Plantaginaceae)

Investigation of the genetic system of six species ofPlantago has revealed striking differences in their breeding and meiotic systems.Plantago patagonica is an inbreeder on account of preanthesis cleistogamy, whereasP. lanceolata is an obligate outbreeder, as it is self-incompatible.Plantago drummondii, P. lagopus, P. ovata, andP. major show mixed mating but in varying proportions. In terms of their energy budgets, outbreeding species invest more in floral advertisement and male function, while inbreeders invest more in female function. The contribution of the meiotic system to genetic variability, as revealed through recombination index, is more important in the inbreeding species.     

Inbreeding and outbreeding depression in Caenorhabditis nematodes

The nematode Caenorhabditis elegans reproduces primarily by self-fertilization of hermaphrodites, yet males are present at low frequencies in natural populations (androdioecy). The ancestral state of C. elegans was probably gonochorism (separate males and females), as in its relative C. remanei. Males may be maintained in C. elegans because outcrossed individuals escape inbreeding depression. The level of inbreeding depression is, however, expected to be low in such a highly selfing species, compared with an outcrosser like C. remanei. To investigate these issues, we measured life-history traits in the progeny of inbred versus outcrossed C. elegans and C. remanei individuals derived from recently isolated natural populations. In addition, we maintained inbred lines of C. remanei through 13 generations of full-sibling mating. Highly inbred C. remanei showed dramatic reductions in brood size and relative fitness compared to outcrossed individuals, with evidence of both direct genetic and maternal-effect inbreeding depression. This decline in fitness accumulated over time, causing extinction of nearly 90% of inbred lines, with no evidence of purging of deleterious mutations from the remaining lines. In contrast, pure strains of C. elegans performed better than crosses between strains, indicating outbreeding depression. The results are discussed in relation to the evolution of androdioecy and the effect of mating system on the level of inbreeding depression.     

Mate choice, genetic incompatibility, and outbreeding in the ornate dragon lizard, Ctenophorus ornatus

There has been recent interest in the role genetic incompatibility may play in mate or sperm choice. One source of incompatibility may be too similar or disparate genomes. An isolated population of the ornate dragon lizard, Ctenophorus ornatus, was followed over a breeding season and parentage assigned to the offspring using microsatellites. It was found that the adults in the population had an eight per cent chance of mating with a relative. I examined whether C. ornatus mate (or fertilize their eggs) with respect to genetic similarity. There was no difference in a female's relatedness to the male in whose territory she resided and her average relatedness to all other males. Neither was there a difference in the relatedness of the male that sired a female's offspring and the female's average relatedness to all other males. There was no evidence of a cost to mating with a more genetically similar mate, because offspring survival was not influenced by degree of inbreeding or outbreeding. However, females that were more outbred had fewer offspring survive. In this small population there are two possible explanations for the decreased fitness associated with outbreeding. First, the species may have an evolutionary history of inbreeding and thus may be susceptible to outbreeding depression. Second. as fitter individuals produce more offspring, these offspring have an increased probability of breeding with relatives, leading to an indirect relationship between fitness and outbreeding.     

Active inbreeding in a cichlid fish and its adaptive significance

Levels of inbreeding are highly variable in natural populations. Inbreeding can be due to random factors (like population size), limited dispersal, or active mate choice for relatives. Because of inbreeding depression, mating with kin is often avoided, although sometimes intermediately related individuals are preferred (optimal outbreeding). However, theory predicts that the advantages of mating with close kin can override the effects of inbreeding depression, but in the animal kingdom, empirical evidence for this is scarce. Here we show that both sexes of Pelvicachromis taeniatus, an African cichlid with biparental brood care, prefer mating with unfamiliar close kin over nonkin, suggesting inclusive fitness advantages for inbreeding individuals. Biparental care requires synchronous behavior among parents. Since parental care is costly, there is a conflict between parents over care, which can reduce offspring fitness. Relatedness is expected to enhance cooperation among individuals. The comparison of the parental behavior of in- and outbreeding pairs showed that related parents were more cooperative and invested more than unrelated parents. Since we found no evidence for inbreeding depression, our results suggest that in P. taeniatus, inbreeding is an advantageous strategy.