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Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression.

The evolutionary transition from outcrossing to self-fertilization has far-reaching implications for patterns of intraspecific genetic diversity and the potential for speciation. Using DNA sequence variation at two nuclear loci, we examined the divergence history of two closely related species of Mimulus. To investigate the effects of mating system and introgressive hybridization on the outcrossing M. guttatus and the selfing M. nasutus, we inspected nucleotide diversity within and between natural populations spanning the species' geographic ranges. High sequence similarity among populations of the selfing M. nasutus points to a single evolutionary origin for the species. Consistent with their distinct mating systems, all genetic variation in M. nasutus is distributed among populations, whereas M. guttatus exhibits appreciable levels of nucleotide diversity within populations. Silent genetic diversity is extensive in M. guttatus (mean theta(sil)/site = 0.077) and greatly exceeds the predicted twofold elevation in neutral variation for outcrossers relative to selfers. The finding of several M. guttatus sequences that share complete identity with sequences from M. nasutus suggests that recent asymmetric introgression may have occurred. We argue that exceptionally high nucleotide diversity in M. guttatus is consistent with a long-term history of directional introgression from M. nasutus to M. guttatus throughout the divergence of these two species.

Base Sequence↗

The cost of peripheral males in a brook trout mating system.

A focus on the reproductive contributions of males displaying alternative life histories has neglected the role of size-dependent peripheral males in salmonine mating systems. We documented mating behaviour of brook trout Salvelinus fontinalis, including observations of spawning, over two breeding seasons to determine the mating costs of peripheral males to dominant males (kleptogamy) and females (egg cannibalism). For males and females, the mating costs of peripheral males were substantial because more than half (56%) of all observed brook trout spawnings involved peripheral males. Males that paired with large females experienced a greater incidence of kleptogamy due to increased numbers of peripheral males present. Large males face a conflict when mating in that they prefer to spawn with large females; however, these same females attract numerous males against which the dominant male cannot defend. From paternity studies, we estimated that males that had peripheral males participate in spawning may fertilize, on average, equal numbers of eggs compared to males spawning solely with a smaller female. Females that paired with relatively smaller males had significantly more eggs eaten by peripheral males than females that paired with relatively larger males. Latency to spawn by females increased when paired with a relatively small male, and resulted in females obtaining a larger spawning partner. The observed patterns of size-assortative mating, kleptogamy and cannibalism are discussed in relation to mate choice for this population of brook trout. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

Behavioural flexibility in the mating system buffers population extinction: lessons from the lesser spotted woodpecker Picoides minor.

1. In most stochastic models addressing the persistence of small populations, environmental noise is included by imposing a synchronized effect of the environment on all individuals. However, buffer mechanisms are likely to exist that may counteract this synchronization to some degree. 2. We have studied whether the flexibility in the mating system, which has been observed in some bird species, is a potential mechanism counteracting the synchronization of environmental fluctuations. Our study organism is the lesser spotted woodpecker Picoides minor (Linnaeus), a generally monogamous species. However, facultative polyandry, where one female mates with two males with separate nests, was observed in years with male-biased sex ratio. 3. We constructed an individual-based model from data and observations of a population in Taunus, Germany. We tested the impact of three behavioural scenarios on population persistence: (1) strict monogamy; (2) polyandry without costs; and (3) polyandry assuming costs in terms of lower survival and reproductive success for secondary males. We assumed that polyandry occurs only in years with male-biased sex ratio and only for females with favourable breeding conditions. 4. Even low rates of polyandry had a strong positive effect on population persistence. The increase of persistence with carrying capacity was slower in the monogamous scenario, indicating strong environmental noise. In the polyandrous scenarios, the increase of persistence was stronger, indicating a buffer mechanism. In the polyandrous scenarios, populations had a higher mean population size, a lower variation in number of individuals, and recovered faster after a population breakdown. Presuming a realistic polyandry rate and costs for polyandry, there was still a strong effect of polyandry on persistence. 5. The results show that polyandry and in general flexibility in mating systems is a buffer mechanism that can significantly reduce the impact of environmental and demographic noise in small populations. Consequently, we suggest that even behaviour that seems to be exceptional should be considered explicitly when predicting the persistence of populations.

Animals↗

Estimation of mating system parameters when outcrossing events are correlated.

Many plant species have mating systems characterized by a mixture of self-fertilization and outcrossing. Statistical estimation of the outcrossing rate has relied on a model of the mating process that assumes that successive outcross events within a family arise from independent draws of pollen from the total population of male plants. Although this assumption is likely to be most appropriate for wind-pollinated plants, it is not appropriate in certain insect-pollinated plants. An alternative model is developed that assumes that successive outcross events within a family involve pollen drawn from a single male parent. The estimation of the parameters that index this model is outlined and a procedure for calculating the variances of the parameter estimates is presented. Monte Carlo simulations of the sampling processes assumed by each model are also presented. The simulations show that application of the incorrect estimation model to data can lead to a large bias in parameter estimates.

Journal Article↗

Variation in the mating system of Vincetoxicum hirundinaria (Asclepiadaceae) in peripherial island populations.

BACKGROUND AND AIMS: Self-fertility may be selected for in small and isolated plant populations of normally outcrossing species. In addition, adaptations for self-fertility are likely to arise in island populations and in populations that are located at the border of the species range. The mating system of Vincetoxicum hirundinaria (Asclepiadaceae) is examined in island populations that are located at the northern border of the species range. METHODS: Pollination experiments were conducted under glasshouse conditions with plants from four populations. KEY RESULTS: The frequencies of self-fertile individuals were relatively high and did not differ among populations. Cross-pollination resulted in higher fruit set than self-pollination. However, fruit-set from self-pollination and cross-pollination did not differ in the self-fertile individuals. Interestingly, the proportion of aborted fruits was on average higher following cross-pollination than following self-pollination. No differences were observed in seed number or seed mass between self- and cross-pollinated fruits. Pollen tube growth following self- and cross-pollinations was indistinguishable. CONCLUSIONS: The results of this study revealed that V. hirundinaria possess a mixed-mating system in the studied island populations. Evidence was also provided for a late-acting self-incompatibility system commonly observed in Asclepiadaceae. No clear signs of inbreeding depression were observed in the early stages of development.

Apocynaceae↗

Deleterious mutation in related species of the plant genus Amsinckia with contrasting mating systems.

Theory for the evolution of modifiers of the rate of mutation suggests that a lower rate of mutation may evolve after the breakdown of mechanisms that enforce outcrossing. Mutation accumulation (MA) experiments were conducted to compare deleterious mutation parameters in two closely related species of the plant genus Amsinckia, a group that exhibits wide variation in the mating system. One of the two species studied (A. douglasiana) is predominantly outcrossed in natural populations, where as the other species (A. gloriosa) is predominantly self-pollinated. Progeny assays of flower number per plant from generation 1 lines (control) and generation 11 lines (MA treatment) were conducted in both species. Dry weight measurements of progeny from the control and MA treatment in A. douglasiana also were made. Estimation of mutation parameters was conducted using maximum likelihood under the assumption of a gamma distribution of mutational effects. The two species exhibited similar rates and effects of deleterious mutation affecting flower number. Estimates of mutation rate for dry weight in A. douglasiana are close to those for flower number. Overall, the estimates of mutation parameters observed in these species are intermediate within the range reported for fitness components in other eukaryotes. The results are discussed within the context of evolutionary change in deleterious mutation accompanying mating system evolution and with respect to previous estimates of mutation parameters based on assays of inbreeding depression and the assumption of mutation-selection equilibrium.

Amsinckia↗

Mammalian mating systems.

Male mammals show a diverse array of mating bonds, including obligate monogamy, unimale and group polygyny and promiscuity. These are associated with a wide variety of different forms of mate guarding, including the defence of feeding and mating territories, the defence of female groups and the defence of individual receptive females. Female mating bonds include long-term monogamy, serial monogamy, polyandry and promiscuity. Both male and female mating behaviour varies widely within species. Variation in male mating behaviour is related to the effect of male assistance in rearing young and to the defensibility of females by males. The latter is, in turn, related to female ranging behaviour and to the size and stability of female groups. Much of the variation in mammalian mating bonds and systems of mate guarding can be attributed to differences in these three variables.

Animals↗

A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.).

The primary objective of this study was to use highly polymorphic microsatellite loci to estimate individual reproductive success in Atlantic salmon based on the number of surviving juveniles (young of the year) at the population level under natural conditions. We inferred reproductive strategies adopted by both sexes by applying a maximum likelihood method to determine parent-offspring genotype relationships. A high degree of variance in individual reproductive success for both males and females was revealed. The high number of mates used by both sexes is not concordant with previous behavioral studies proposing that females are mainly monogamous in this species. We found little evidence supporting the prediction from previous reports of a positive relationship between individual size and realized reproductive success for either males or females. For both sexes, however, there was a significant correlation between the number of mates and the number of offspring. These results indicate that this species' mating system is more flexible than previously thought and suggest that factors such as potential genetic benefits or environmental uncertainty may also be driving the evolution and the plasticity of mating systems in Atlantic salmon.

Alleles↗

Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants.

Parental conflicts can lead to antagonistic coevolution of the sexes and of parental genomes. Within a population, the resulting antagonistic effects should balance, but crosses between populations can reveal conflict. Parental conflict is less intense in self-pollinating plants than in outcrossers because outcrossing plants are pollinated by multiple pollen donors unrelated to the seed parent, while a self-pollinating plant is primarily pollinated by one individual (itself). Therefore, in crosses between plants with differing mating systems, outcrossing parents are expected to "overpower" selfing parents. We call this the weak inbreeder/strong outbreeder (WISO) hypothesis. Prezygotically, such overpowering can alter pollination success, and we argue that our hypothesis explains a common pattern of unilateral incompatibility, in which pollen from self-incompatible populations fertilizes ovules of self-compatible individuals but the reciprocal cross fails. A postzygotic manifestation of overpowering is aberrant seed development due to parent-of-origin effects such as genomic imprinting. We evaluate evidence for the WISO hypothesis by reviewing published accounts of crosses between plants of different mating systems. Many, but not all, of such reports support our hypothesis. Since parental conflicts can perturb fertilization and development, such conflicts may strengthen reproductive barriers between populations, contributing to speciation.

Flowers↗

Mating systems of diploid and allotetraploid populations of Tragopogon (Asteraceae). II. Artificial populations.

Polyploidization has long been recognized as an important force in the diversification of plants. Theoretical models predict that polyploids may be expected to exhibit higher rates of self-fertilization than do closely related diploid species. Wild populations of the neopolyploid Tragopogon mirus (4n) exhibited slightly higher rates of outcrossing than did populations of one of its progenitors, T. dubius (2n). In the current study, outcrossing rates in populations of T. dubius and T. mirus were estimated using artificial arrays constructed to maximize the chances of detecting outcrossing events. The artificial diploid population is more highly outcrossing (t=0.727; family-level estimates range from 0.00 to 1. 32) than the tetraploid population (t=0.591; family-level estimates range from 0.00 to 1.14), although the difference between them is not statistically significant. The results of this study, combined with those of the previous work on wild populations, suggest that mating systems in these species vary more among populations than between ploidal levels. This could be because of the relatively recent origins of the tetraploid species; there may have been insufficient time since the formations of the tetraploids for shifts in mating systems to occur.

Alleles↗

The orang-utan mating system and the unflanged male: A product of increased food stress during the late Miocene and Pliocene?

The orang-utan is unique among apes in having an unusually long male developmental period and two distinct adult male morphs (flanged and unflanged), which generally, but not exclusively, employ different reproductive strategies (call-and-wait vs. sneak-and-rape). Both morphs have recently been shown to have roughly similar levels of reproductive success in the one site where such a study has been conducted. This is in stark contrast to the unimale polygynous gorilla, in which dominant males sire almost all infants. Despite this, evidence on sexual dimorphism, life history, diet, and socioecology of extant and extinct apes, as well as the ontogeny, reproductive morphology, and physiology of extant apes, all indicate that the orang-utan's present-day mating system most likely evolved from a gorilla-like base, with one dominant male guarding a harem of females. The available evidence indicates that, due chiefly to the likely onset of the El Niño Southern Oscillation (generally regarded as the trigger for mast fruiting in dipterocarps) approximately 3-5Ma, southeast Asian forests would have begun to experience longer and more severe periods of low food availability. This change in food availability would have meant that full-time gregariousness was no longer energetically tolerable and, as a result, females dispersed more widely in search of food and adult/flanged males were no longer able to effectively guard a harem of females. A niche for a quiet, quick, opportunistic "sexual predator" (i.e., the unflanged male) then became available. This finding implies that, despite being anatomically quite chimpanzee-like, the ancestral hominoid probably had a social and mating system more similar to the gorilla than any other living ape.

Animals↗

The distribution of plant mating systems: study bias against obligately outcrossing species.

Early models of plant mating-system evolution argued that predominant outcrossing and selfing are alternative stable states. At least for animal-pollinated species, recent summaries of empirical studies have suggested the opposite-that outcrossing rates do not show the expected bimodal distribution. However, it is generally accepted that several potential biases can affect conclusions from surveys of published outcrossing rates. Here, we examine one potential bias and find that published studies of outcrossing rates contain far fewer obligate outcrossers than expected. We approximate the magnitude of this study bias and present the distribution of outcrossing rates after compensating for it. Because this study examines only one potential bias, and finds it to be large, conclusions regarding either the frequency of mixed mating or the shape of the distribution of outcrossing rates in nature are premature.

Crosses, Genetic↗

Sexually transmitted disease and the evolution of mating systems.

Sexually transmitted diseases (STDs) have been shown to increase the costs of multiple mating and therefore favor relatively monogamous mating strategies. We examine another way in which STDs can influence mating systems in species in which female choice is important. Because more popular males are more likely to become infected, STDs can counteract any selective pressure that generates strong mating skews. We build two models to investigate female mate choice when the sexual behavior of females determines the prevalence of infection in the population. The first model has no explicit social structure. The second model considers the spatial distribution of matings under social monogamy, when females mated to unattractive males seek extrapair fertilizations from attractive males. In both cases, the STD has the potential to drastically reduce the mating skew. However, this reduction does not always happen. If the per contact transmission probability is low, the disease dies out and is of no consequence. In contrast, if the transmission probability is very high, males are likely to be infected regardless of their attractiveness, and mating with the most attractive males imposes again no extra cost for the female. We also show that optimal female responses to the risk of STDs can buffer the prevalence of infection to remain constant, or even decrease, with increasing per contact transmission probabilities. In all cases considered, the feedback between mate choice strategies and STD prevalence creates frequency-dependent fitness benefits for the two alternative female phenotypes considered (choosy vs. randomly mating females or faithful vs. unfaithful females). This maintains mixed evolutionarily stable strategies or polymorphisms in female behavior. In this way, a sexually transmitted disease can stabilize the populationwide proportion of females that mate with the most attractive males or that seek extrapair copulations.

Choice Behavior↗

Mating behavior and endocrine profiles of wild black and white Colobus monkeys (Colobus guereza): toward an understanding of their life history and mating system.

Black and white colobus monkeys (Colobus guereza, "guerezas") show no external signs of estrus, and little is known about their mating behavior or reproductive endocrinology. To learn more about the life history characteristics and mating system of guerezas, we documented the mating behavior and ovarian hormone profiles of 10 cycling, lactating, and pregnant females in a wild population. We studied six groups of guerezas in Kibale National Park, Uganda, and collected ad libitum data on their mating behavior. We collected urine samples every 1.9+/-0.2 days from potentially fertile females and quantified conjugated urinary estrogen (E1S) and progesterone (PdG) metabolites using enzyme immunoassay (EIA). Females solicited 50.5% of copulations, and most copulations occurred during the interval starting 5 days before presumptive ovulation and ending 2-3 days later, with the highest copulatory levels occurring close to ovulation. We show that the median ovarian cycle length is 24 days, the median gestation length is approximately 158 days, the length of lactational amenorrhea is at least 7-8 months, and the median interbirth interval for females with surviving infants is approximately 22 months. We also document overlap between females' receptive periods in one-male, two- to three-female groups, which may mean that male transfer into such groups is potentially profitable.

Amenorrhea↗

Mating system parameters of Dryobalanops aromatica Gaertn. f. (Dipterocarpaceae) in three different forest types and a seed orchard.

The mating system of Dryobalanops aromatica in three different forest types and a seed orchard was quantified by allozyme analysis of progeny arrays using a mixed-mating model. The primary forest (Bukit Sai) had the highest multilocus outcrossing rate (tm=0.923 +/- 0.035), followed by logged forest (Lesong; tm=0.766 +/- 0.056) and artificial forest (FRIM; tm=0.661 +/- 0.066) with seed orchard showing the lowest (Tampin; tm=0.551 +/- 0.095). Deviations from the mixed mating model were evident from differences in pollen and ovule allele frequencies, and heterogeneity of pollen pools in all three different forest types and the seed orchard. A high rate of outcrossing in primary forest (tm=0.92) may indicate that the species is self-incompatible, but a lower value in the seed orchard (tm=0.55) might suggest further that the self-incompatibility system is weak. The outcrossing rate was greater in the primary forest (tm=0.92) than in logged forest (tm=0.77). It is argued that this might be a consequence of the lower density of flowering trees and alteration of pollinator foraging behaviour in logged forest. Higher values of correlated mating (rp) and biparental mating (tm - ts) in primary forest (0.08 and 0.39, respectively) in comparison with logged forest (0.03 and 0.11, respectively) demonstrate that logging activities might reduce the seeds produced through consanguineous mating. Compared with primary forest, it is argued that lower rates of outcrossing in artificial forest (tm=0.67) and seed orchard (tm=0. 55) might be attributed to lack of flowering synchrony and insufficient number of pollinators. The high level of correlated mating (rp=0.43) and biparental mating (tm - ts=0.12) in the seed orchard may further suggest that the seed orchard was established using related seed sources.

Crosses, Genetic↗

Sex-biased predation by polecats influences the mating system of frogs.

In agile frogs, Rana dalmatina, an increase in male-biased operational sex ratio and in male abundance results in the emergence of alternative male mating behaviour in the form of searching. As a consequence, females are coerced into mating with multiple males, which in turn increases the level of conflict between the sexes. Selective predation on males by the European polecat, Mustela putorius, decreases the occurrence of polyandry. In ponds visited by polecats, the sex ratio is less male biased than in ponds where polecats are absent. As a result most males call to attract females and fewer males actively search for females. Females are able to choose between calling males and mate with a single male. Thus, predation by polecats is found to influence sex ratio, male abundance and sexual conflict in a frog mating system, restricting the opportunity for multiple mating.

Animals↗

Impacts of forest fragmentation on the mating system and genetic diversity of white spruce (Picea glauca) at the landscape level.

We studied the mating system of white spruce (Picea glauca) in a landscape fragmented by agriculture in northern Ontario, Canada. We sampled 23 stands that ranged in size from 1 to >500 trees isolated by 250-3000 m from the nearest other stand. Six polymorphic allozyme loci from four enzyme systems were used to genotype approximately 10 000 embryos from 104 families. We detected no allele frequency heterogeneity in the pollen pool among stands or families (Phi(FT)=-0.025). Overall, estimates of outcrossing were high (t(m)=94% and mean t(s)=91%) but significantly different from unity. Bi-parental inbreeding (t(m)-t(s)=3.2%) was low but significantly different from zero. Allozyme-based outcrossing estimates did not differ significantly among three stand-size classes (SSCs): small (<10 trees), medium (10-100 trees) and large (> or =100 trees). The number of effective pollen donors was high in all SSCs, but was significantly lower in small stands (N(ep)=62.5) than in medium-sized and large stands (both N(ep)=143). The primary selfing rate was significantly higher in medium stands than in large stands. We found no significant difference in genetic diversity measures in the filial (seed) population among SSCs. Overall, these results indicate that white spruce stands in this fragmented landscape are resistant to genetic diversity losses, primarily through high pollen-mediated gene-flow and early selection against inbred embryos. We discuss the importance of using seed data, in conjunction with genetic data, to evaluate the impacts of fragmentation on natural populations.

Canada↗

Behavioural aspects of the raccoon mating system: determinants of consortship success.

We monitored raccoons Procyon lotor, in southern Texas during the 1990-1992 mating seasons to describe mating behaviour and identify factors affecting consortship success. During most of this study, raccoons were spatially aggregated, with female home ranges congregated around permanent water sources and larger home ranges of male groups encompassing each female group. Consortship success varied among males and ranged from zero to six females per male within a mating season. Individual females consorted with one to four different males during an oestrous period; however, most (62%) females consorted with only one male during their oestrus. Dominance through overt conflict appeared to influence male consortship success. During two mating seasons, one male from each group consorted with females on more days than all other males combined. Body weight of males was positively correlated with number of consortship days. As synchrony of oestrus increased, variance in number of consortship days among males decreased, and access to oestrous females increased for subordinate males. Wounding among males increased during the mating season, and was more frequent for males than for females. The mating system, as determined by consortship behaviour, appeared to shift between polygyny and promiscuity, and possibly varied annually as a result of the timing of oestrous cycles. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗