Promiscuity in sand lizards (Lacerta agilis) and adder snakes (Vipera berus): causes and consequences

We review postcopulatory phenomena in the Swedish sand lizard (Lacerta agilis) and adder (Vipera berus), and in particular, links between female promiscuity, determinants of paternity, and offspring viability. In both species, females mate multiply and exhibit a positive relationship between the number of partners and offspring viability. We conclude that this relationship is most likely the result of variable genetic compatibility between mates arising from postcopulatory phenomena, predominantly assortative fertilization with respect to parental genotypes. However, males who were more successful at mate acquisition were also more successful in situations of sperm competition, suggesting a possible link between male (diploid and haploid) genetic quality per se and probability of fertilization. Neither the number of partners nor the number of matings influenced the risk of infertility in sand lizards, suggesting that selection for reduced risk of infertility is not a sufficient explanation for maintaining female promiscuity in this population. Finally, we conclude that the relatively low genetic variability exhibited by our study populations may have facilitated detection of genetic benefits compared to more outbred ones. However, recent work derived from outbred populations in other taxa suggest a greater generality of the principles we discuss than previously may have been appreciated.     

Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii

Recent work has confirmed that genetic compatibility among mates can be an important determinant of siring success in sperm competition experiments and in free-ranging populations. Most of this work points towards mate choice of less related mates. However, there may also be the potential for mate choice for intermediate or even genetically similar mates to prevent outbreeding depression or hybridization with closely related taxa. We studied relatedness effects on post-copulatory gametic choice and/or sperm competition in an external fertilizer, Peron's tree frog (Litoria peronii), since external fertilizers offer exceptional control in order to test gametic interaction effects on probability of paternity and zygote viability. Sperm competition experiments were done blindly with respect to genetic relatedness among males and females. Thereafter, paternity of offspring was assigned using eight microsatellite loci. Three hybridization trials between L. peronii and a closely related sympatric species Litoria tyleri were also carried out. In the sperm competition trials, males that are more genetically similar to the female achieved higher siring success compared with less genetically similar males. The hybridization trials confirmed that the two species can interbreed and we suggest that the risk of hybridization may contribute to selection benefits for genetically more similar males at fertilization. To our knowledge, this study is the first to show evidence for post-copulatory selection of sperm from genetically more similar individuals within a natural population.     

No evidence of sperm selection by female common shrews.

There is currently much interest in the suggestion that females are capable of post-copulatory (or cryptic) choice for male genetic compatibility. Here, I investigate this idea using data from mixed-paternity litters of the common shrew (Sorex araneus). Females of this species are highly promiscuous and, in natural populations, regularly incur costs of inbreeding by mating with close relatives. Selection should therefore favour female ability for sperm selection on the basis of male relatedness. No evidence was found in support of this idea. Relative number of offspring sired within mixed paternity litters was not significantly correlated with genetic similarity of males to the female mated. Relative fertilization success was, however, significantly related to male epididymal sperm counts. I conclude that most variation in relative fertilization success of male common shrews can be explained in terms of sperm competition, and that females of this species may not be capable of sperm selection.     

The more pieces,the better the puzzle: sperm concentration increases gametic compatibility

The genetic benefits individuals receive from mate choice have been the focus of numerous studies, with several showing support for both intrinsic genetic benefits and compatibility effects on fertilization success and offspring viability. However, the robustness of these effects have rarely been tested across an ecologically relevant environmental gradient. In particular, sperm environment is a crucial factor determining fertilization success in many species, especially those with external fertilization. Here, we test the importance of sperm environment in mediating compatibility‐based selection on fertilization using a factorial breeding design. We detected a significant intrinsic male effect on fertilization success at only one of four sperm concentrations. Compatibility effects were significant at the two highest sperm concentrations and, interestingly, the magnitude of the compatibility effect consistently increased with sperm concentration. This suggests that females are able to modify the probability of sperm–egg fusion as the amount of sperm available increases.     

Fitness consequences of parental compatibility in the frog Crinia georgiana

Theory suggests that multiple mating by females can evolve as a mechanism for acquiring compatible genes that promote offspring fitness. Genetic compatibility models predict that differences in fitness among offspring arise from interactions between male and female haplotypes. Using a cross-classified breeding design and in vitro fertilization, we raised families of maternal and paternal half-siblings of the frog Crinia georgiana, a species with a polyandrous breeding system and external fertilization. After controlling for variation in maternal provisioning, we found significant effects of interacting parental haplotypes on fertilization success, and nonadditive genetic effects on measures of offspring fitness such as embryo survival, and survival to, size at, and time to metamorphosis. Additive genetic variation due to males and females was negligible, and not statistically significant for any of the fitness traits measured. Combinations of parental haplotypes that resulted in high rates of fertilization produced offspring with higher embryo survival and rapid juvenile development. We suggest that a gamete recognition mechanism for selective fertilization by compatible sperm may promote offspring fitness in this system.     

Offspring sex ratio under inbreeding and outbreeding in a gynodioecious plant

Silene vulgaris is a gynodioecious plant native to Eurasia and now found throughout much of North America. Using hermaphrodite plants from three geographic regions (Stamford, NY; Broadway,VA; and Giles Co., VA) and four local populations within each region, we employed a hierarchical crossing design to explore the geographic structure of sex determining genes. Sex determination in this species is cytonuclear involving multiple cytoplasmic male sterility and nuclear restorer loci. Due to dominance effects within nuclear restorer loci, self-fertilization of hermaphrodites heterozygous at restorer loci should produce some homozygous recessive female offspring. Female offspring may also result from outcrossing among related individuals. At greater geographic and genetic distances, mismatches between cytoplasmic and nuclear sex determining genes should also produce high frequencies of female offspring if coevolution between cytoplasmic and nuclear sex determining alleles occurs independently among widely separated populations. We found evidence of dominance effects among nuclear restorer loci but no evidence of nuclear-cytoplasmic mismatches at the regional level. Of 63 maternal lines, 55 produced at least one female offspring when self-fertilized. Outcrossing within populations produced significantly fewer female offspring than self-fertilization. Outcrossing among regions produced the lowest proportion of female offspring, significantly fewer than outcrossing among populations within regions. Regions responded differently to among-region outcrossing with pollen donors from the two Virginia regions producing far fewer female offspring with New York dams than crosses among New York populations. These results indicate that nuclear restoration is complex, involving multiple loci with epistatic interactions and that most hermaphrodites in nature are heterozygous at one or more restorer locus. Further, regional differences in restorer frequencies indicate significant genetic structure for sex determining genes at large geographic scales, perhaps reflecting invasion history.     

How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).     

Cryptic preference for MHC-dissimilar females in male red junglefowl,Gallus gallus

An increasing number of studies test the idea that females increase offspring fitness by biasing fertilization in favour of genetically compatible partners; however, few have investigated or controlled for corresponding preferences in males. Here, we experimentally test whether male red junglefowl, Gallus gallus, prefer genetically compatible females, measured by similarity at the major histocompatibility complex (MHC), a key gene complex in vertebrate immune function. Theory predicts that because some degree of MHC heterozygosity favours viability, individuals should prefer partners that carry MHC alleles different from their own. While male fowl showed no preference when simultaneously presented with an MHC-similar and an MHC-dissimilar female, they showed a ‘cryptic’ preference, by allocating more sperm to the most MHC-dissimilar of two sequentially presented females. These results provide the first experimental evidence that males might respond to the MHC similarity of a female through differential ejaculate expenditure. By revealing that cryptic male behaviours may bias fertilization success in favour of genetically compatible partners, this study demonstrates the need to experimentally disentangle male and female effects when studying preferences for genetically compatible partners.     

Covariance among premating, post-copulatory and viability fitness components in Drosophila melanogaster and their influence on paternity measurement

In polyandrous mating systems, male fitness depends on success in premating, post-copulatory and offspring viability episodes of selection. We tracked male success across all of these episodes simultaneously, using transgenic Drosophila melanogaster with ubiquitously expressed green fluorescent protein (i.e. GFP) in a series of competitive and noncompetitive matings. This approach permitted us to track paternity-specific viability over all life stages and to distinguish true competitive fertilization success from differential early offspring viability. Relationships between episodes of selection were generally not present when paternity was measured in eggs; however, positive correlations between sperm competitive success and offspring viability became significant when paternity was measured in adult offspring. Additionally, we found a significant male × female interaction on hatching success and a lack of repeatability of offspring viability across a focal male's matings, which may underlay the limited number of correlations found between episodes of selection.     

Decreased sexual signalling reveals reduced viability in small populations of the drumming wolf spider Hygrolycosa rubrofasciata

One of the important goals in conservation biology is to determine reliable indicators of population viability. Sexual traits have been suggested to indicate population extinction risk, because they may be related to viability through condition dependence. Moreover, condition-dependent sexual traits may be more sensitive indicators of population viability than early life-history traits, because deleterious fitness effects of inbreeding tend to be expressed mainly at the end of the species' life history. However, empirical evidence of the significance of sexual behaviour for population viability is missing. In this study, we examined two male sexual traits and survival in 39 different-sized and isolated natural populations of the wolf spider, Hygrolycosa rubrofasciata. We also used several traits to estimate female reproductive success in 25 populations of H. rubrofasciata. According to previous studies, H. rubrofasciata males have a costly and condition-dependent acoustic signal, courtship drumming, which is the target of female choice. Males with a high drumming rate have considerably higher viability than males with a low drumming rate, and females that mate with the more actively drumming males gain genetic benefits in terms of increased offspring viability. Our results show that males in small populations had both lower survival and lower drumming rate than males in larger populations. However, we did not find any evidence for a decline in important early life-history traits (offspring number, hatching success or offspring body mass) or female body mass in small populations. Our results have two important messages for conservation biology. First, they show that sexual traits can be used as sensitive indicators of population viability. Second, the indirect benefits of female choice in terms of good genes might partially compensate for the reduction of viability in declining populations. Also, our results support the view that deleterious effects of small population size are expressed at the end of the species' life history.     

Sources of phenotypic variance in egg and larval traits in a marine invertebrate

Contrary to many separate sex systems, the evolutionary ecology of polyandry in simultaneous hermaphrodites, and in particular in those with internal fertilization, has received little attention. Recent studies on the promiscuous gastropod Chelidonura sandrana showed that offspring size, an important determinant of offspring performance in many marine invertebrates, varies with the number of different mating partners. However, the source of this differential allocation by mothers remained unclear. Using a quantitative genetic model, we here tested for parental effects on offspring size and the importance of ‘good gene’ effects on early life history traits. Our analysis revealed no significant sire but strong dam effects for all investigated traits. Moreover, embryo viability tended to increase with egg capsule volume, thus linking offspring size with offspring performance. Our findings suggest that in C. sandrana (1) differential allocation is a maternal effect in response to the number of different partners, and that (2) additive genetic variance is of negligible importance in early life history traits.     

Notes on African Mosses. I. Andreaea camerunensis sp.nov. and other Mosses mostly from Nigeria and the British Cameroons

Abstract

Reproductive ecological traits such as success of fertilization, partitioning of sexes, the relative success of sexual versus asexual reproduction and dispersal distances are likely to considerably influence genetic structure within and among plant populations. In the liverwort Mannia fragrans both sexual and asexual reproduction can be frequently observed: sporophytes are produced abundantly every year and asexual propagation by fragmentation of thalli is also common. The aim of this study was to use ecological and molecular methods (ISSR markers) to separate the role of sexual and asexual components in shaping the partitioning of genetic variability within and among populations. In addition to genetic analyses conducted seasonally, sex expression and fertilization rates, sex ratios, regeneration from vegetative fragments and outcrossing was estimated in 3 populations of the species. Sex expression rates were high and, in spite of strongly female biased sex ratios, high fertilization rates were detected. However, capacity for regeneration from fragments was also high. Despite frequent spore production genetic diversity was low within populations. This is probably the result of the predominance of asexual reproduction s. 1. including crossing between genetically identical plants. Although recombination and mutation occasionally generates new haplotypes, these have little chance to spread because of the large spores mainly falling into their own patch, where chances for germination are low. Due to small size and isolation of the populations, genetic drift is likely to eliminate these haplotypes. Remote populations differed significantly, each being dominated by a few clones, reflecting negligible gene flow among them. Differences among individual populations can partly be related to differences in their reproductive behaviour and degree of isolation.     

She gets many and she chooses the best: polygynandry in Salamandrina perspicillata (Amphibia: Salamandridae)

Polyandry is a widespread mating strategy, found in a broad number of taxa. Among amphibians, polyandry, and multiple paternity as its direct consequence, is quite common in salamanders, especially within Ambystomatidae and Plethodontidae. In the suborder Salamadroidea the existence of two different types of spermatheca allows several kinds of polyandry strategies to appear. We used multilocus microsatellite genotyping to investigate the presence of polyandry and its effects on the paternity in a previously unstudied species with a terrestrial habit, Salamandrina perspicillata. We collected gravid females in their natural habitat and analysed the paternity of the offspring by using the software COLONY and GERUD. We found that all the analysed clutches had been fertilized by 2–4 males and that in every clutch one male had sired most of the offspring. Our results confirmed that polyandry is an important component of the mating system of this species, suggesting that females are able to recognize the sperm of the male that will provide a genetic benefit for their offspring. We found evidence of female cryptic choice based on males' genetic dissimilarity: (1) males who sire most of the offspring of a given female tend to be genetically different from their sexual partner; (2) a same male, when mated with two females, sired a proportion of the offspring inversely correlated with his genetic similarity to the female; (3) genetic dissimilarity between mating partners is positively correlated with offspring heterozygosity. According to the genetic compatibility model, we hypothesized that in the observed non resource‐based mating system the indirect benefit for the offspring should reflect interactions between paternal and maternal genomes rather than the inheritance of the so‐called ‘good genes’. This study suggests a polygynandrous mating system for the study species and provides the first report in a salamandrid species in natural condition that reproductive success of males is correlated with genetic dissimilarity between mates. Moreover, we found evidence of an offspring benefit (higher heterozygosity) derived from the most genetically dissimilar father.     

Fitness Benefits of Mate Choice for Compatibility in a Socially Monogamous Species

Research on mate choice has primarily focused on preferences for quality indicators, assuming that all individuals show consensus about who is the most attractive. However, in some species, mating preferences seem largely individual-specific, suggesting that they might target genetic or behavioral compatibility. Few studies have quantified the fitness consequences of allowing versus preventing such idiosyncratic mate choice. Here, we report on an experiment that controls for variation in overall partner quality and show that zebra finch (Taeniopygia guttata) pairs that resulted from free mate choice achieved a 37% higher reproductive success than pairs that were forced to mate. Cross-fostering of freshly laid eggs showed that embryo mortality (before hatching) primarily depended on the identity of the genetic parents, whereas offspring mortality during the rearing period depended on foster-parent identity. Therefore, preventing mate choice should lead to an increase in embryo mortality if mate choice targets genetic compatibility (for embryo viability), and to an increase in offspring mortality if mate choice targets behavioral compatibility (for better rearing). We found that pairs from both treatments showed equal rates of embryo mortality, but chosen pairs were better at raising offspring. These results thus support the behavioral, but not the genetic, compatibility hypothesis. Further exploratory analyses reveal several differences in behavior and fitness components between “free-choice” and “forced” pairs.     

The evolution of polyandry: intrinsic sire effects contribute to embryo viability

Females typically mate with more than one male despite the costs incurred, thus questioning Bateman's principle. A series of genetic benefits have been proposed to account for the evolution of polyandry, including the acquisition of viability genes for offspring. The 'intrinsic male quality' hypothesis suggests that polyandry increases the probability that females produce offspring sired by males that bestow high viability on their offspring. Heritable variation in viability is the basic requirement for the occurrence of this genetic benefit. By using a half-sib breeding design with a species of cricket in which polyandry is known to increase hatching success, we present clear experimental evidence that intrinsic male quality contributes to embryo viability. Despite recent support for the evolution of polyandry based on compatibility of genotypes between males and females, we show that hatching success is not determined by an interaction between paternal and maternal genotypes but rather that sons inherit paternal genes that influence the viability of eggs laid by their mates. Moreover, our data implicate a potential role for indirect genetic effects of male accessory gland products on embryo viability. Additive genetic contributions to embryo viability may be an important factor underlying the frequently observed benefits of polyandrous behaviour.     

Female effects,but no intrinsic male effects on paternity outcome in crickets

Competitive fertilization success can depend on the relative abilities of competing males to fertilize available ova, and on mechanisms of cryptic female choice that moderate paternity. Competitive fertilization success is thus an emergent property of competing male genotypes, female genotype and their interactions. Accurate estimates of intrinsic male effects on competitive fertilization success are therefore problematic. We used a cross‐classified nonbreeding design in which rival male family background was standardized to partition variation in competitive fertilization success among male and female family backgrounds in the field cricket Teleogryllus oceanicus. Male effects were close to zero, supporting previous quantitative genetic designs in which male competitors were assigned at random. In contrast, some 22% of the variance in competitive fertilization success was explained by female effects, suggesting that paternity in this species is influenced strongly by cryptic female choice.     

High levels of multiple paternity in Littorina saxatilis: hedging the bets?

The mating system of a species can have great effects on its genetic structure and evolution. We studied the extent of multiple paternity in a gastropod with internal fertilization, the intertidal snail Littorina saxatilis. Paternal genotype reconstruction based on microsatellite markers was performed on the offspring of wild, naturally fertilized females from 2 populations. The numbers of males contributing to the offspring per female were among the highest detected in invertebrates so far, with the exception of social insects. No reproductive skew in favor of males that were genetically more distant from the females was detected, and the pattern of fertilization appeared random. The result fits a hypothesis of indiscriminate mating, with genetic bet hedging as the most likely explanation. Bet hedging may have evolved as a form of inbreeding avoidance, if the snails are not able to recognize relatives. However, nutritional benefits from sperm or sexual conflict with males are additional possibilities that remain to be assessed in this species. Whatever the causes, such high levels of multiple paternity are remarkable and are likely to have a large impact on population structure and dynamics in a species in which migration between populations is spurious.     

Parental effects on fertilization and hatching success and development of Atlantic halibut (Hippoglossus hippoglossus L.) embryos and larvae

The parental effects on fertilization and early life history traits were studied in Atlantic halibut, Hippoglossus hippoglossus L. Sperm from 12 different males were used to fertilize eggs of two females in separate crosses. The fertilization success were generally high, above 80% of developing embryos at 16-cell stage in 20 of 24 crosses with an average of 85.9+/-17.6% and 87.2+/-16.5% for female A and female B, respectively. Corresponding hatching success was 74.8+/-17.7% and 41.6+/-20.1%, respectively. The relationship between fertilization success and hatching success was positive. The parental influence on hatching was dominated by a strong and significant (p<0.001) maternal effect; however, the paternal effect was also significant (p<0.001). Furthermore, there was no relationship between fertilization success, hatching success and larvae viability as a high number of larvae developed locked jaws (i.e., were not functional). There was a significant (p<0.01) difference in yield of functional larvae of female A (43%) and female B (56%), and also between crosses sired by different males. The standard length of offspring of female A (12.4+/-0.5 mm) and B (12.6+/-0.6 mm) were significantly (p<0.001) different, and also significantly influenced by both the female (p<0.001) and the male (p<0.001). The present paper provides strong indications that not only the female, but also the male parent influences quantitative features of early development of their offspring.     

Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae)

Self-incompatibility systems function to prevent inbreeding, and work effectively in large, genetically diverse populations. However, a decrease in population size can reduce genetic diversity at the self-incompatibility locus, which leads to a reduction in mate availability and has important demographic implications for small populations. Currently, little is known about the response of self-incompatible polyploid species to a reduction in population size. In Rutidosis leptorrhynchoides there was a significant decrease in the within-population probability of fertilization with a decline in population size for diploid populations and a marginally significant relationship for tetraploid populations, suggesting that in small populations of both chromosome races fertilization success is reduced due to a decrease in self-incompatibility allele (S-allele) diversity. There was no significant difference between the slopes of the fertility-population size relationship for diploid and tetraploid populations which indicates a similar rate of decline in fertilization success with population size for both chromosome races. Fertilization success increased when crosses were undertaken between populations and this was significantly related to population size for diploid and tetraploid populations, indicating that small populations gain the greatest benefit to fertilization success from crossing between populations. For tetraploid populations the benefits of crossing between populations tended to decline more rapidly with increasing population size. These results suggest that for small populations that have reduced fertilization success, genetic rescue by introducing new genetic material from other populations is an important means of ameliorating mate limitation issues associated with reduced S-allele diversity in both diploid and tetraploid races.     

Parental identity influences progeny responses to incubation thermal stress in sockeye salmon Onchorhynchus nerka

The influence of individual parentage on progeny responses to early developmental temperature stress was examined in a cross-fertilization experiment using sockeye salmon Oncorhynchus nerka. Differences in survival, hatch timing and size were examined among five paternally linked and five maternally linked offspring families (Weaver Creek population, British Columbia, Canada) incubated at 12, 14 and 16° C from just after fertilization to hatch. Mean embryonic survival was significantly lower at 14 and 16° C; however, offspring families had substantially different survival responses across the thermal gradient (crossing reaction norms). Within temperature treatments, substantial variation in embryonic survival, alevin mass, time-to-hatch and hatch duration were attributable to family identity; however, most traits were governed by significant temperature-family interactions. For embryonic survival, large differences between families at 16° C were due to both female and male spawner influence, whereas inter-family differences were obscured at 14° C (high intra-family variation), and minimal at 12° C (only maternal influence detected). Despite post-hatch rearing under a common cool thermal regime, persistent effects of both temperature and parentage were detected in alevin and 3 week-old fry. Collectively, these findings highlight the crucial role that parental influences on offspring may have in shaping future selection within salmonid populations exposed to elevated thermal regimes. An increased understanding of parental and temperature influences and their persistence in early development will be essential to developing a more comprehensive view of population spawning success and determining the adaptive capacity of O. nerka populations in the face of environmental change.