Selfing and resource allocation in Schiedea salicaria (Caryophyllaceae), a gynodioecious species

Abstract Levels of selfing and resource allocation patterns were investigated in Schiedea salicaria (Caryophyllaceae), a gynodioecious species with high levels of inbreeding depression and nuclear control of male sterility. Selfing levels were higher in hermaphrodites than females, especially when adjusted for early acting inbreeding depression. The sexes of S. salicaria were similar in most allocation patterns including number of flowers and capsules per inflorescence, seeds per flower, and seed mass. Seeds produced by females had higher levels of germination than seeds of hermaphrodites, a likely result of high selfing levels and the expression of inbreeding depression in the progeny of hermaphrodites. Invasion of females in populations of S. salicaria is probably related to the expression of inbreeding depression at germination and in later life history stages. Comparisons with related species of Schiedea that also have nuclear control of male sterility suggest that reallocation of resources in hermaphrodites to male function occurs as females increase in frequency, but that resource reallocation is not important for the success of females when they first invade populations.     

Close‐kin mating,but not inbred parents,reduces hatching rates and offspring quality in a threatened tortoise

Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long‐lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long‐lived species is limited. In this study, we leverage a well‐studied population of gopher tortoises, Gopherus polyphemus, to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long‐lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex‐specific evolutionary trade‐offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long‐lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.     

Mating system contributes only slightly to female maintenance in gynodioecious Geranium maculatum (Geraniaceae)

Gynodioecy, the co-occurrence of female and hermaphroditic individuals within a population, is an important intermediate in the evolution of separate sexes. The first step, female maintenance, requires females to have higher seed fitness compared with hermaphrodites. A common mechanism thought to increase relative female fitness is inbreeding depression avoidance, the magnitude of which depends on hermaphroditic selfing rates and the strength of inbreeding depression. Less well studied is the effect of biparental inbreeding on female fitness. Biparental inbreeding can affect relative female fitness only if its consequence or frequency differs between sexes, which could occur if sex structure and genetic structure both occur within populations. To determine whether inbreeding avoidance and/or biparental inbreeding can account for female persistence in Geranium maculatum, we measured selfing and biparental inbreeding rates in four populations and the spatial genetic structure in six populations. Selfing rates of hermaphrodites were low and did not differ significantly from zero in any population, leading to females gaining at most a 1–14% increase in seed fitness from inbreeding avoidance. Additionally, although significant spatial genetic structure was found in all populations, biparental inbreeding rates were low and only differed between sexes in one population, thereby having little influence on female fitness. A review of the literature revealed few sexual differences in biparental inbreeding among other gynodioecious species. Our results show that mating system differences may not fully account for female maintenance in this species, suggesting other mechanisms may be involved.     

Does inbreeding avoidance maintain gender dimorphism in Wurmbea dioica (Colchicaceae)?

The maintenance of females in gender dimorphic populations requires that they have a fitness advantage to compensate for their loss of male reproductive function. We assess whether inbreeding avoidance provides this advantage in two subdioecious Wurmbea dioica populations by estimating seed production, outcrossing rates and inbreeding depression. Fruiting males produced less than half as many seeds as females, owing to low outcrossing rates and early acting inbreeding depression. Inbreeding coefficients of fruiting males demonstrated that progeny were more inbred than their parents, implying that few selfed progeny reach maturity, as confirmed by inbreeding depression estimates that exceeded 0.85. In a glasshouse experiment, open-pollinated females exhibited a fitness advantage of 3.7 relative to fruiting males, but when we increased fruiting male outcrossing rate, female advantage was only 1.4. This reduced advantage is insufficient to maintain females if nuclear genes control sex. Thus, inbreeding avoidance could maintain females at high frequencies, although this is contingent upon high frequencies of fruiting males, which can be altered by environmentally determined gender plasticity.     

Inbreeding avoidance through kin recognition: choosy females boost male dispersal

Inbreeding avoidance is predicted to induce sex biases in dispersal. But which sex should disperse? In polygynous species, females pay higher costs to inbreeding and thus might be expected to disperse more, but empirical evidence consistently reveals male biases. Here, we show that theoretical expectations change drastically if females are allowed to avoid inbreeding via kin recognition. At high inbreeding loads, females should prefer immigrants over residents, thereby boosting male dispersal. At lower inbreeding loads, by contrast, inclusive fitness benefits should induce females to prefer relatives, thereby promoting male philopatry. This result points to disruptive effects of sexual selection. The inbreeding load that females are ready to accept is surprisingly high. In absence of search costs, females should prefer related partners as long as delta相似文献   

Gender-specific inbreeding depression in a gynodioecious plant, Geranium maculatum (Geraniaceae)

In gynodioecious species, females coexist with hermaphrodites in natural populations even though hermaphrodites attract more pollinators, are capable of reproducing through pollen, and can self-fertilize. This study tests the hypothesis that inbreeding depression helps to maintain females in natural populations. It also examines whether gender lineages that differ in selfing rates might experience different levels of inbreeding depression. Female and hermaphroditic lineages of the gynodioecious species Geranium maculatum were used in self, sib-cross and outcross experiments to examine inbreeding depression levels and to determine whether these levels differ between hermaphroditic and female lineages. Six fitness correlates were measured in the greenhouse and compared among pollination types and between genders. Severe inbreeding depression was found for both individual fitness traits and cumulative fitness in early life history stages. Inbreeding depression levels were slightly higher in hermaphroditic than in female lineages, but this difference was not statistically significant. Because females are unable to self-pollinate and are less likely to experience inbreeding than hermaphrodites under natural conditions, these results suggest that severe inbreeding depression could confer a selective advantage for females that could help to maintain females in natural populations.     

Mating system, sex ratio, and persistence of females in the gynodioecious shrub Daphne laureola L. (Thymelaeaceae)

Although in gynodioecious populations male steriles require a fecundity advantage to compensate for their gametic disadvantage, southern Spanish populations of the long-lived shrub Daphne laureola do not show any fecundity advantage over hermaphrodites in terms of seed production and early seedling establishment. By using allozyme markers, we assess the mating system of this species in five populations differing in sex ratio, and infer levels of inbreeding depression over the whole life cycle by comparing the inbreeding coefficients at the seed and adult plant stages. Extremely low outcrossing rates (0.001相似文献   

Marker-based investigation of inbreeding depression in the endangered species Brassica insularis

Various methods have been proposed to estimate inbreeding depression and to assess its consequences for natural populations. As an alternative to controlled crosses, the use of molecular markers has allowed direct investigation of inbreeding depression in natural populations, but usually suffers from low statistical power. Here, we investigated the effect of inbreeding depression on survival in two populations of the rare species Brassica insularis, using both controlled crosses and a marker-based approach. We compare the respective merits of the two approaches for studying inbreeding depression. We also use information from the molecular markers to dissect in detail patterns of inbreeding depression in this species. A posteriori, we find that combining the approaches was not necessary to obtain simple point estimates of inbreeding depression. However, using molecular markers may give insight into the genetic basis of inbreeding depression, such as the occurrence of epistatic interactions among deleterious alleles or purging.     

Pollination biology and outcrossing rates in hermaphroditic Schiedea lydgatei (Caryophyllaceae)

The influence of outcrossing and pollination biology on the maintenance of hermaphroditism was studied for Schiedea lydgatei (Caryophyllaceae: Alsinoideae), a species endemic to Moloka`i in the Hawaiian Islands. Schiedea lydgatei is the only hermaphroditic species in an otherwise dimorphic clade and hermaphroditism is likely the result of a reversal from a gynodioecious ancestor. Both wind and native moths in the family Pyralidae are responsible for pollination in S. lydgatei. Outcrossing rates were generally high (0.80), especially in years when the greatest number of plants were flowering. The combination of high outcrossing rates and substantial inbreeding depression indicates that at present females would not be favored in the population. Pollination by both wind and insects is consistent with the hypothesis that hermaphroditism is the result of a relatively recent reversal, as the ancestor of S. lydgatei was probably wind pollinated and gynodioecious with few females in the populations. A shift from wind to predominately insect pollination on Moloka`i may have resulted in increased outcrossing rates and prevented the expression of high inbreeding depression among progeny of hermaphrodites, a condition that would select against females and favor a reversal to hermaphroditism. Because few females were likely to have been present in ancestral populations that colonized Moloka`i, founder effect is another potential explanation for loss of females. In either case, current high levels of outcrossing prevent re-establishment of females in populations of S. lydgatei.     

Moderate inbreeding depression in a reintroduced population of North Island robins

Reintroductions of threatened species are increasingly common in conservation. The translocation of a small subset of individuals from a genetically diverse source population could potentially lead to substantial inbreeding depression due to the high genetic load of the parent population. We analysed 12 years of data from the reintroduced population of North Island robins Petroica longipes on Tiritiri Matangi Island, New Zealand, to determine the frequency of inbreeding and magnitude of inbreeding depression. The initial breeding population consisted of 12 females and 21 males, which came from a large mainland population of robins. The frequency of mating between relatives ( f >0; 39%, n =82 pairs) and close relatives ( f =0.25; 6.1%) and the average level of inbreeding ( f =0.027) were within the range reported for other small island populations of birds. The average level of inbreeding fluctuated from year to year depending on the frequency of close inbreeding (e.g. sib–sib pairs). We found evidence for inbreeding depression in juvenile survival, with survival probability estimated to decline from 31% among non-inbred birds ( f =0) to 11% in highly inbred juveniles ( f =0.25). The estimated number of lethal equivalents based on this relationship (4.14) was moderate compared with values reported for other island populations of passerines. Given that significant loss of fitness was only evident in highly inbred individuals, and such individuals were relatively rare once the population expanded above 30 pairs, we conclude that inbreeding depression should have little influence on this robin population. Although the future fitness consequences of any loss of genetic variation due to inbreeding are uncertain, the immediate impact of inbreeding depression is likely to be low in any reintroduced population that expands relatively quickly after establishment.     

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.     

No evidence of inbreeding avoidance in a polygynous ungulate: the reindeer (Rangifer tarandus)

In polygynous species, mate choice is an integrated part of sexual selection. However, whether mate choice occurs independently of the genetic relatedness among mating pairs has received little attention, although inbreeding may have fitness consequences. We studied whether genetic relatedness influenced females' choice of partner in a highly polygynous ungulate--the reindeer (Rangifer tarandus)--in an experimental herd during two consecutive rutting seasons; the herd consisting of 75 females in 1999 and 74 females in 2000 was exposed to three 4.5-year-old adults and three 1.5-year-old young males, respectively. The females' distribution during peak rut was not influenced by their genetic relatedness with the dominant males of the mating groups. Further, genetic relatedness did not influence the actual choice of mating partner. We conclude that inbreeding avoidance through mating group choice as well as choice of mating partner, two interconnected processes of female mate choice operating at two different scales in space and time, in such a highly female-biased reindeer populations with low level of inbreeding may not occur.     

Inbreeding depression by recessive deleterious genes affecting female fecundity of a haplo‐diploid mite

The effect of inbreeding on haplo‐diploid organisms has been regarded as very low, because deleterious recessive genes on hemizygous (haploid) males were immediately purged generation by generation. However, we determined such recessive genes to decrease female fecundity in a population of Schizotetranychus miscanthi Saito which is known in the Acari as a subsocial species with haplo‐diploidy. In mother–son inbreeding experiments, there was no depression in egg hatchability nor in the larval survival of progeny over four generations. There was, on the other hand, significant inbreeding depression in the fecundity with increasing f‐value. Crosses between two lineages, one having deleterious effects on the fecundity and the other having no such effects, established during the inbreeding, revealed heterosis, and backcrosses showed that the depression was caused by deleterious recessive(s). These results strongly suggest the existence of some deleterious genes governing only the traits of adult females in wild populations of haplo‐diploid organisms.     

Cryptic behaviours, inverse genetic landscapes, and spatial avoidance of inbreeding in the Pacific jumping mouse

Although the behaviour of individuals is known to impact the genetic make-up of a population, observed behavioural patterns do not always correspond to patterns of genetic structure. In particular, philopatric or dispersal-limited species often display lower-than-expected values of relatedness or inbreeding suggestive of the presence of cryptic migration, dispersal, or mating behaviours. I used a combination of microsatellite and mark-recapture data to test for the influence of such behaviours in a dispersal-limited species, the Pacific jumping mouse, within a semi-isolated population over three seasons. Despite short dispersal distances and a low rate of first generation migrants, heterozygosities were high and inbreeding values were low. Dispersal was male-biased; interestingly however, this pattern was only present when dispersal was considered to include movement away from paternal home range. Not unexpectedly, males were polygynous; notably, some females were also found to be polyandrous, selecting multiple neighbouring mates for their single annual litter. Patterns of genetic structure were consistent with these more inconspicuous behavioural patterns. Females were more closely related than males and isolation by distance was present only in females. Furthermore, detailed genetic landscapes revealed the existence of strong, significant negative correlations, with areas of low genetic distance among females overlapping spatially with areas of high genetic distance among males. These results support the hypothesis that the detected cryptic components of dispersal and mating behaviour are reducing the likelihood of inbreeding in this population through paternally driven spatial mixing of male genotypes and polyandry of females.     

Moderate multiple parentage and low genetic variation reduces the potential for genetic incompatibility avoidance despite high risk of inbreeding

Background

Polyandry is widespread throughout the animal kingdom. In the absence of direct benefits of mating with different males, the underlying basis for polyandry is enigmatic because it can carry considerable costs such as elevated exposure to sexual diseases, physical injury or other direct fitness costs. Such costs may be balanced by indirect genetic benefits to the offspring of polyandrous females. We investigated polyandry and patterns of parentage in the spider Stegodyphus lineatus. This species experiences relatively high levels of inbreeding as a result of its spatial population structure, philopatry and limited male mating dispersal. Polyandry may provide an opportunity for post mating inbreeding avoidance that reduces the risk of genetic incompatibilities arising from incestuous matings. However, multiple mating carries direct fitness costs to females suggesting that genetic benefits must be substantial to counter direct costs.

Methodology/Principal Findings

Genetic parentage analyses in two populations from Israel and a Greek island, showed mixed-brood parentage in approximately 50% of the broods. The number of fathers ranged from 1–2 indicating low levels of multiple parentage and there was no evidence for paternity bias in mixed-broods from both populations. Microsatellite loci variation suggested limited genetic variation within populations, especially in the Greek island population. Relatedness estimates among females in the maternal generation and potentially interacting individuals were substantial indicating full-sib and half-sib relationships.

Conclusions/Significance

Three lines of evidence indicate limited potential to obtain substantial genetic benefits in the form of reduced inbreeding. The relatively low frequency of multiple parentage together with low genetic variation among potential mates and the elevated risk of mating among related individuals as corroborated by our genetic data suggest that there are limited actual outbreeding opportunities for polyandrous females. Polyandry in S. lineatus is thus unlikely to be maintained through adaptive female choice.     

MIXED MATING SYSTEMS IN HAWAIIAN BIDENS (ASTERACEAE)

Floral features related to the breeding system were studied for 11 species of Hawaiian Bidens. Protandry and male sterility promote outcrossing, while self-compatibility and geitonogamy contribute to inbreeding. The combination of these floral mechanisms results in a mixed mating system in all species studied. Outcrossing rates of 15 populations of these species ranged from 0.43 to 0.88, averaging 0.65. Apparent selling rates of females ranged from 0 to 0.25 in seven gynodioecious populations surveyed, suggesting that there is variation in the level of biparental inbreeding among populations. The presence of females increased the level of outcrossing by an average of 9% in gynodioecious populations. This study indicates that the efficiency of gynodioecy as an outcrossing mechanism largely depends on the current outcrossing rate of hermaphrodites, the frequency of females, and the extent of genetic substructuring in populations. On average, autogamy contributed 4%, geitonogamy contributed 24%, and consanguineous mating contributed 15% to the realized selfing rate (43%) in the hermaphrodites of these species.     

The imprecision of heterozygosity-fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species

In nonpedigreed wild populations, inbreeding depression is often quantified through the use of heterozygosity-fitness correlations (HFCs), based on molecular estimates of relatedness. Although such correlations are typically interpreted as evidence of inbreeding depression, by assuming that the marker heterozygosity is a proxy for genome-wide heterozygosity, theory predicts that these relationships should be difficult to detect. Until now, the vast majority of empirical research in this area has been performed on generally outbred, nonbottlenecked populations, but differences in population genetic processes may limit extrapolation of results to threatened populations. Here, we present an analysis of HFCs, and their implications for the interpretation of inbreeding, in a free-ranging pedigreed population of a bottlenecked species: the endangered takahe (Porphyrio hochstetteri). Pedigree-based inbreeding depression has already been detected in this species. Using 23 microsatellite loci, we observed only weak evidence of the expected relationship between multilocus heterozygosity and fitness at individual life-history stages (such as survival to hatching and fledging), and parameter estimates were imprecise (had high error). Furthermore, our molecular data set could not accurately predict the inbreeding status of individuals (as 'inbred' or 'outbred', determined from pedigrees), nor could we show that the observed HFCs were the result of genome-wide identity disequilibrium. These results may be attributed to high variance in heterozygosity within inbreeding classes. This study is an empirical example from a free-ranging endangered species, suggesting that even relatively large numbers (>20) of microsatellites may give poor precision for estimating individual genome-wide heterozygosity. We argue that pedigree methods remain the most effective method of quantifying inbreeding in wild populations, particularly those that have gone through severe bottlenecks.     

A new theory for the evolution of polyandry as a means of inbreeding avoidance

We propose a novel theory for the evolution of polyandry driven by genetic benefits to females whose offspring interbreed. In species with an ecology characterized by frequent colonization of new habitat patches, consanguineous matings may be common during the early stages of colonization, but genetic diversity may grow as new colonizers arrive. We show that with levels of inbreeding depression similar to those found in predominantly inbreeding populations, a polyandrous female can benefit her descendants since matings among her brood are mainly between half siblings rather than full siblings. We examine the invasion by a polyandrous phenotype using explicit genetic models in which costs of inbreeding are themselves subject to selection. In common with other models of inbreeding, we find that underlying high levels of inbreeding tend to purge deleterious recessive alleles, and hence these are unlikely to maintain sufficient inbreeding depression to favour polyandry. However, if costs of inbreeding are due to overdominance, biologically realistic levels of inbreeding depression result in genetic benefits large enough to favour polyandry provided it is not too costly. The potential significance of polyandry as a mechanism to reduce inbreeding in grandchildren will depend upon the genetic basis of inbreeding depression in natural, inbreeding populations.     

How much better are females? The occurrence of female advantage,its proximal causes and its variation within and among gynodioecious species

Background

Gynodioecy is a reproductive system of interest for evolutionary biologists, as it poses the question of how females can be maintained while competing with hermaphrodites that possess both male and female functions. One necessary condition for the maintenance of this polymorphism is the occurrence of a female advantage, i.e. a better seed production or quality by females compared with hermaphrodites. Theoretically, its magnitude can be low when sterility mutations are cytoplasmic, while a 2-fold advantage is needed in the case of nuclear sterility. Such a difference is often thought to be due to reduced inbreeding depression in obligatory outcrossed females. Finally, variation in sex ratio and female advantage occur among populations of some gynodioecious species, though the prevalence of such variation is unknown.

Scope

By reviewing and analysing the data published on 48 gynodioecious species, we examined three important issues about female advantage. (1) Are reduced selfing and inbreeding depression likely to be the major cause of female advantage? (2) What is the magnitude of female advantage and does it fit theoretical predictions? (3) Does the occurrence or the magnitude of female advantage vary among populations within species and why?

Conclusions

It was found that a female advantage occurred in 40 species, with a magnitude comprised between 1 and 2 in the majority of cases. In many species, reduced selfing may not be a necessary cause of this advantage. Finally, female advantage varied among populations in some species, but both positive and negative correlations were found with female frequency. The role of reduced selfing in females for the evolution of gynodioecy, as well as the various processes that affect sex ratios and female advantage in populations are discussed.     

Maternal-zygotic gene conflict over sex determination: effects of inbreeding

There is growing evidence that sex determination in a wide range of organisms is determined by interactions between maternal-effect genes and zygotically expressing genes. Maternal-effect genes typically produce products (e.g., mRNA or proteins) that are placed into the egg during oogenesis and therefore depend upon maternal genotype. Here it is shown that maternal-effect and zygotic genes are subject to conflicting selective pressures over sex determination in species with partial inbreeding or subdivided populations. The optimal sex ratios for maternal-effect genes and zygotically expressing genes are derived for two models: partial inbreeding (sibmating) and subdivided populations with local mating in temporary demes (local mate competition). In both cases, maternal-effect genes are selected to bias sex determination more toward females than are zygotically expressed genes. By investigating the invasion criteria for zygotic genes in a population producing the maternal optimum (and vice versa), it is shown that genetic conflict occurs between these genes. Even relatively low levels of inbreeding or subdivision can result in maternal-zygotic gene conflict over sex determination. The generality of maternal-zygotic gene conflict to sex determination evolution is discussed; such conflict should be considered in genetic studies of sex-determining mechanisms.