Can paternal effects via seminal fluid contribute to the evolution of polyandry?

Genetic benefits from mating with multiple males are thought to favour the evolution of polyandry. However, recent evidence suggests that non-genetic paternal effects via seminal fluid might contribute to the observed effects of polyandry on offspring performance. Here, we test this hypothesis using the field cricket Teleogryllus oceanicus. Using interference RNA, we first show that at least one seminal fluid protein is essential for embryo survival. We then show that polyandrous females mated to three different males produced embryos with higher pre-hatching viability than did monandrous females mated with the same male three times. Pseudo-polyandrous females that obtained sperm and seminal fluid from a single male and seminal fluid from two additional males had embryos with viabilities intermediate between monandrous and polyandrous females. Our results suggest either that ejaculate mediated paternal effects on embryo viability have both genetic and non-genetic components, or that seminal fluids transferred by castrated males provide only a subset of proteins contained within the normal ejaculate, and are unable to exert their full effect on embryo viability.     

Genetic variance of mating frequency in the honeybee (Apis mellifera L.)

Summary. The genetic variance of queen mating frequency was studied in honeybees (Apis mellifera carnica). Worker offspring (N = 966) of 28 naturally mated half sister-queens (r = 0.25) from seven unrelated breeding lines were genotyped at four DNA microsatellites. The mating frequencies of the queens were derived from the offspring genotypes. The number of observed matings per queen ranged from 10 to 28 with an average of 17.32 ± 1.10 (number of estimated matings: 24.94 ± 2.51; number of effective matings: 20.09 ± 1.73). Half-sib analyses of the breeding lines were used to estimate heritability. Heritability was h² = 0.449 ± 0.135 for the estimated number of matings and h² = 0.262 ± 0.103 for the number of effective males, which are both significantly different from zero. We conclude that a high genetic variance for polyandry in honeybees can be favored by balanced selection between individual queen and colony level.Received 16 October 2003; revised 4 May 2004; accepted 4 May 2004.     

An empirical test of the bet‐hedging polyandry hypothesis: Female red flour beetles avoid extinction via multiple mating

Bet‐hedging via polyandry (spreading the extinction risk of the female''s lineage over multiple males) may explain the evolution of female multiple mating, which is found in a wide range of animal and plant taxa. This hypothesis posits that females can increase their fitness via polyandrous mating when “unsuitable” males (i.e., males causing reproductive failure for various reasons) are frequent in the population and females cannot discriminate such unsuitable mates. Although recent theoretical studies have shown that polyandry can operate as a bet‐hedging strategy, empirical tests are scarce. In the present study, we tested the bet‐hedging polyandry hypothesis by using the red flour beetle Tribolium castaneum. We compared female reproductive success between monandry and polyandry treatments when females mated with males randomly collected from an experimental population, including 20% irradiated (infertile) males. In addition, we evaluated geometric mean fitness across multiple generations as the index of adaptability of bet‐hedging traits. Polyandrous females showed a significantly higher egg hatching rate and higher geometric mean fitness than monandrous females. These results strongly support the bet‐hedging polyandry hypothesis.     

Paternity costs from polyandry compensated by increased fecundity in the hide beetle

Polyandry-induced sperm competition is assumed to impose costson males through reduced per capita paternity success. In contrast,studies focusing on the consequences of polyandry for femalesreport increased oviposition rates and fertility. For thesespecies, there is potential for the increased female fecundityassociated with polyandry to offset the costs to males of sharedpaternity. We tested this hypothesis by comparing the proportionand number of offspring sired by males mated with monandrousand polyandrous females in the hide beetle, Dermestes maculates,both for males mating with different females and for males rematingwith the same female. In 4 mating treatments, monandrous femalesmated either once or twice with the same male and polyandrousfemales mated either twice with 2 different males or thricewith 2 males (where 1 male mated twice). Polyandrous and twice-matingmonandrous females displayed greater fecundity and fertilitythan singly mating monandrous females. Moreover, males rematedto the same female had greater paternity regardless of whetherthat female mated with another male. In both polyandrous treatments,male mating order did not affect paternity success. Finally,although the proportion of eggs sired decreased if a male matedwith a polyandrous female, multiply mating females or femalesthat remated with a previous mate laid significantly more eggsand thus the actual number of eggs sired was comparable. Thus,males do not necessarily accrue a net fitness loss when matingwith polyandrous females. This may explain the absence of anyobvious defensive paternity-protection traits in hide beetlesand other species.     

Benefits of polyandry in Parthenium beetle,Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae)

The influence of polyandry on the reproductive performance of females and on offspring fitness in Zygogramma bicolorata Pallister was investigated using four experimental treatments, viz. (A) monandrous, limited mating, (B) monandrous, unlimited mating, (C) polyandrous, no-choice limited mating, and (D) polyandrous, mate choice unlimited mating. Polyandrous females had higher reproductive performance than monandrous ones. Monandrous females subjected to unlimited matings had higher egg viability than those subjected to limited matings, but fecundity did not differ significantly. In polyandrous females, the freedom to choose mates did not affect reproductive performance. However, offspring of polyandrous females allowed mate choice developed fastest and had the highest survival at 25, 27, and 30 °C. Thus, polyandry in Z. bicolorata appears to provide both direct (material) and indirect (genetic) benefits resulting in better reproductive performance and increased adaptability of the offspring to counter environmental stresses. The present study not only adds to the knowledge of reproductive biology of Z. bicolorata but it could also be of economic value as it may help in the mass rearing of Z. bicolorata and in the management of Parthenium hysterophorus.     

Repeated mating with the same male increases female longevity and fecundity in a polyandrous leaf beetle Galerucella birmanica (Coleoptera: Chrysomelidae)

Female multiple mating (polyandry) is widespread across Insecta, even if mating can be costly to females. To explain the evolution and maintenance of polyandry, several hypotheses, mainly focusing on the material (direct) and/or the genetic (indirect) benefits, have been proposed and empirically tested in many species. Considering only the direct benefits, repeatedly‐mated females are expected to exhibit the same fitness as multiply‐mated females under the same mating frequency. In the present study, we compare the fitness of females received monandrous repeated mating (MM) and polyandrous multiple mating (PM) in a polyandrous leaf beetle Galerucella birmanica and assess female mate preference with regard to polyandry or monandry. Our data indicate that the longevity and the egg‐laying duration of MM females are significantly longer than that of PM females. MM females produce significantly more hatched eggs than PM females over their lifetime under the same mating frequency, which results from the high hatching rate of eggs produced by MM females. PM females mated with novel virgin males in the second mating suffer decreased longevity and lifetime fecundity compared with PM females mated with novel mated males in the second mating. Once‐mated females are more likely to re‐mate with familiar males than novel males. By contrast to expectations, the results of the present study suggest that repeated mating provides females with more direct benefits than multiple mating in G. birmanica, and females prefer to re‐mate with familiar males. The possible causes of this finding are discussed.     

Life history tradeoffs in relation to the degree of polyandry and developmental pathway in Pieris napi (Lepidoptera, Pieridae)

Pieris napi females have different heritable reproductive tactics. Polyandrous females have higher lifetime fecundity, whereas monandrous ones start to reproduce at a faster rate. Butterfly larvae are time‐constrained in seasonal environments. Thus, polyandry is expected to be associated with fast juvenile development, which may result in biased mortality due to physiological costs. We compared how females with varying degrees of polyandry allocate between duration of larval period and achievable size in directly developing and over‐wintering generations. Offspring survival and growth were monitored under a high density and low quality diet. Polyandrous females developed at a faster rate than monandrous ones, regardless of developmental pathway. The growth rate of female offspring correlated with their mothers’ degree of polyandry, which underpins polyandry and monandry as distinct strategies with life history differences reaching beyond mating frequency. The high growth rate of polyandrous females resulted in a short larval period among directly developing females, and in large size within an over‐wintering cohort. A change in either the duration of the larval period or pupal mass had no significant effect on the other, emphasising that growth rate is not necessarily a simple outcome of the tradeoff between development time and size at maturity. The correlation between the degree of polyandry and juvenile growth rate diminished when larvae were exposed to environmental stress, which offers an explanation why juvenile mortality was decoupled from mating tactic. We conclude that polyandry is a strategy that allows larvae to utilise optimal conditions in a more effective way than monandry. As a consequence, polyandrous females either achieve larger size or they mature faster. This gives them a double advantage over monandrous ones within an over‐wintering generation or diminishes the effects of asynchronous hatching of offspring within a directly developing generation. Possible costs of high growth rate are discussed.     

Polyandrous females provide sons with more competitive sperm: Support for the sexy‐sperm hypothesis in the rattlebox moth (Utetheisa ornatrix)

Given the costs of multiple mating, why has female polyandry evolved? Utetheisa ornatrix moths are well suited for studying multiple mating in females because females are highly polyandrous over their life span, with each male mate transferring a substantial spermatophore with both genetic and nongenetic material. The accumulation of resources might explain the prevalence of polyandry in this species, but another, not mutually exclusive, possibility is that females mate multiply to increase the probability that their sons will inherit more‐competitive sperm. This latter “sexy‐sperm” hypothesis posits that female multiple mating and male sperm competitiveness coevolve via a Fisherian runaway process. We tested the sexy‐sperm hypothesis by using competitive double matings to compare the sperm competition success of sons of polyandrous versus monandrous females. In accordance with sexy‐sperm theory, we found that in 511 offspring across 17 families, the male whose polyandrous mother mated once with each of three different males sired significantly more of all total offspring (81%) than did the male whose monandrous mother was mated thrice to a single male. Interestingly, sons of polyandrous mothers had a significantly biased sex ratio of their brood toward sons, also in support of the hypothesis.     

Material and genetic benefits of female multiple mating and polyandry

The maintenance of female polyandry has traditionally been attributed to the material (direct) benefits derived from male mating resources (e.g. nuptial gifts) accrued by multiple mating. However, genetic (indirect) benefits offer a more robust explanation since only polyandrous, not monandrous, females may gain both material benefits from multiple mating and genetic benefits from multiple sires. Discriminating between material and genetic benefits is essential when addressing the mechanism by which polyandry is adaptively maintained, but are difficult to disentangle because they affect fitness in similar ways. To test the hypothesis that genetic benefits maintain polyandry, we compared four components of fitness (longevity, fecundity, hatching success and survivorship) between monandrous and polyandrous females in the ground cricket, Allonemobius socius. We discovered that females derived nongenetic benefits from mating multiply, in that the magnitude of the nuptial gift was positively associated with the number of eggs produced. However, polyandrous females had over a two-fold greater hatching success and a 43% greater offspring survivorship, leading to a significantly higher relative fitness than the monandrous strategy. These results were independent of the confounding effects of material benefits, implying that genetic contributions play a large role in the maintenance of polyandry and potentially in the antagonistic coevolutionary relationship between polyandry and male nuptial gifts. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour     

Inheritance of Cry1Ac resistance and associated biological traits in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae)

The analysis of reciprocal genetic crosses between resistant Helicoverpa armigera strain (BH-R) (227.9-fold) with susceptible Vadodara (VA-S) strain showed dominance (h) of 0.65-0.89 and degree of dominance (D) of 0.299-0.782 suggesting Cry1Ac resistance as a semi-dominant trait. The D and h values of F₁ hybrids of female resistant parent were higher than female susceptible parent, showing maternally enhanced dominance of Cry1Ac resistance. The progeny of F₂ crosses, backcrosses of F₁ hybrid with resistant BH-R parent did not differ significantly in respect of mortality response with resistant parent except for backcross with female BH-R and male of F₁ (BH-R × VA-S) cross, suggesting dominant inheritance of Cry1Ac resistance. Evaluation of some biological attributes showed that larval and pupal periods of progenies of reciprocal F₁ crosses, backcrosses and F₂ crosses were either at par with resistant parent or lower than susceptible parent on treated diet (0.01 μg/g). The susceptible strain performed better in terms of pupation and adult formation than the resistant strain on untreated diet. In many backcrosses and F₂ crosses, Cry1Ac resistance favored emergence of more females than males on untreated diet. The normal larval period and the body weight (normal larval growth) were the dominant traits associated with susceptible strain as contrast to longer larval period and the lower body weight (slow growth) associated with resistance trait. Further, inheritance of larval period in F₂ and backcross progeny suggested existence of a major resistant gene or a set of tightly linked loci associated with Cry1Ac sensitivity.     

A sex allocation cost to polyandry in a parasitoid wasp

The costs and benefits of polyandry are central to understanding the near-ubiquity of female multiple mating. Here, we present evidence of a novel cost of polyandry: disrupted sex allocation. In Nasonia vitripennis, a species that is monandrous in the wild but engages in polyandry under laboratory culture conditions, sexual harassment during oviposition results in increased production of sons under conditions that favour female-biased sex ratios. In addition, females more likely to re-mate under harassment produce the least female-biased sex ratios, and these females are unable to mitigate this cost by increasing offspring production. Our results therefore argue that polyandry does not serve to mitigate the costs of harassment (convenience polyandry) in Nasonia. Furthermore, because males benefit from female-biased offspring sex ratios, harassment of ovipositing females also creates a novel cost of that harassment for males.     

Unifying selection acts on competitive ability and relative growth rate in Scabiosa columbaria

Q_ST vs. F_ST comparisons can reveal diversifying or unifying selection pressures among populations for specific traits. In this study we performed Q_ST–F_ST analyses on eleven populations of Scabiosa columbaria from the Swiss Jura to reveal genetic differentiation in two quantitative traits (above-ground biomass and relative growth rate of leaf lengths) and in neutral molecular markers. Above-ground biomass of plants under competition has been shown to correlate with their competitive ability, which is an important fitness-related trait. We hypothesized that strong unifying selection acts on above-ground biomass, since underperformance would result in decreased fitness and overperformance is unlikely due to trade-offs with other plant functions.Overall G_ST (an F_ST analogue) was 0.12. Analysis of variance revealed that above-ground biomass and relative growth rate did not differ among populations, but both traits differed among seed families and were heritable (h² = 0.31 and h² = 0.35, respectively). Q_ST was close to zero for above-ground biomass and zero for relative growth rate of leaf lengths, and thus Q_ST was much lower than G_ST, indicating unifying selection on these traits.This conclusion is restricted by the limits of the used methodology. Q_ST < F_ST cannot always be considered as a proof for unifying selection, because in complex traits the assumption of purely additive effects of underlying genes may be violated. However, given the large differences between Q_ST and G_ST, together with substantial heritabilities of the traits under study, we conclude that our findings are not in contradiction with the hypothesis of unifying selection.     

Monandry and polyandry as alternative lifestyles in a butterfly

Butterflies show considerable variability in female mating frequency, ranging from monandrous species to females mating several timesin their lifetime. Degree of polyandry also varies within species,with some females only mating once and others mating multiply.Previous studies have shown that one reason for female multiplemating is to obtain nutritious male donations that both increasethe longevity of females and result in higher lifetime fecundity.Despite the presence of male nutrient donations, some femalesof the green-veined white butterfly (Pieridae: Pieris napi)never mate more than once. In this study, we examined thisapparent paradox. We assessed to what degree polyandry is undergenetic control by a full-sib analysis, and we also estimatedthe broad sense heritability of female lifetime fecundity in singly mated females. Both polyandry and lifetime fecundityhave a genetic component. However, degree of polyandry appearsto be traded off against reduced longevity when denied theopportunity to mate more than once. It is possible that femaleP. napi display different reproductive strategies, with somefemales relying on male donations to realize their potentialfecundity and others relying on their own resources for egg production. In nature, polyandrous females may be preventedfrom mating multiply due to unfavorable weather. We discussthe possibility that the trade-off between degree of polyandryand life span when singly mated may affect the maintenanceof genetic variability in female mating frequency in this species.Possible reasons for these different reproductive strategiesare discussed.     

The effect of interspecific mating on sex ratios in the twospotted spider mite and the Banks grass mite (Acarina: Tetranychidae)

Mixed populations of the twospotted spider mite (TSM),Tetranychus urticae (Koch), and the Banks grass mite (BGM),Oligonychus pratensis (Banks), occur on corn and sorghum plants in late summer in the Great Plains. Interspecific matings between these arrhenotokous species occur readily in the laboratory but yield no female offspring. The effect of interspecific mating on female: male sex ratios was measured by examining the F₁ progeny of females that mated with both heterospecific and conspecific males in no-choice situations. TSM females that mated first with BGM males and then with TSM males produced a smaller percentage of female offspring than TSM females that mated only with TSM males (43.1±5.8 and 78.9±2.8% females, respectively). Similarly, BGM females mated with heterospecific males and then with conspecific males produced fewer female offspring than females mated only with BGM males (55.7±5.2 and 77.5±2.5%, respectively). Lower female: male sex ratios were produced also by BGM females that mated with TSM males after first mating with conspecifics (62.4±3.4%). In mixed populations containing males of both species, females also produced lower female: male sex ratios, but these ratios were not as low as expected based on mating propensities and progeny sex ratios observed in no-choice tests. These data suggest that interspecific mating may substantially reduce female fitness in both mite species by reducing the output of female offspring, but in mixed populations this effect is mitigated by unidentified behavioral mechanisms.     

Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank voles Clethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those of monandrous females. This was mainly due to sons of polyandrous females producing significantly more offspring than those of monandrous females. No significant differences were found for offspring body mass or winter survival between the two treatments. Our results appear to provide evidence that bank vole females gain long-term benefits from polyandry.     

Mating portfolios: bet-hedging,sexual selection and female multiple mating

Polyandry (female multiple mating) has profound evolutionary and ecological implications. Despite considerable work devoted to understanding why females mate multiply, we currently lack convincing empirical evidence to explain the adaptive value of polyandry. Here, we provide a direct test of the controversial idea that bet-hedging functions as a risk-spreading strategy that yields multi-generational fitness benefits to polyandrous females. Unfortunately, testing this hypothesis is far from trivial, and the empirical comparison of the across-generations fitness payoffs of a polyandrous (bet hedger) versus a monandrous (non-bet hedger) strategy has never been accomplished because of numerous experimental constraints presented by most ‘model’ species. In this study, we take advantage of the extraordinary tractability and versatility of a marine broadcast spawning invertebrate to overcome these challenges. We are able to simulate multi-generational (geometric mean) fitness among individual females assigned simultaneously to a polyandrous and monandrous mating strategy. Our approaches, which separate and account for the effects of sexual selection and pure bet-hedging scenarios, reveal that bet-hedging, in addition to sexual selection, can enhance evolutionary fitness in multiply mated females. In addition to offering a tractable experimental approach for addressing bet-hedging theory, our study provides key insights into the evolutionary ecology of sexual interactions.     

Testing the viviparity-driven-conflict hypothesis: parent-offspring conflict and the evolution of reproductive isolation in a poeciliid fish

The evolution of viviparity increases the potential for genomic conflicts between mothers and offspring over the level of maternal investment. The viviparity-driven-conflict hypothesis predicts that such conflicts will drive the evolution of asymmetrical reproductive isolation between populations with divergent mating systems. We tested this hypothesis using crosses between populations of a poeciliid fish that differ in their level of polyandry. Our results support the prediction of an asymmetry in the rate of spontaneous abortion in reciprocal crosses, with the highest rate occurring in crosses between females from a relatively monandrous population and males from a relatively polyandrous population. The patterns of offspring size were not consistent with the pattern predicted by the viviparity-driven-conflict hypothesis: crosses between a monandrous female and a polyandrous male did not produce larger offspring than the reciprocal cross. This discrepancy was due to the presence of an effect of the maternal population on offspring size: polyandrous females produced larger offspring than monandrous females. In addition, offspring size was positively correlated with maternal size in crosses involving a polyandrous male. We discuss these results in light of models for intra- and intergenomic epistasis and the rapid origin of asymmetric reproductive isolation in viviparous taxa.     

Good genes and the maternal effects of polyandry on offspring reproductive success in the bulb mite

Genetic benefits are potentially the most robust explanation of the controversial issue of evolutionary maintenance of polyandry, but the unambiguous demonstration of such benefits has been hindered by the possibility of their confusion with maternal effects. Previous research has shown that polyandrous bulb mite females produce daughters with higher fecundity than monandrous females. Here, we investigate whether this effect arises because polyandrous females invest more in their offspring, or because their offspring inherit 'good genes' from their fathers. Females were mated with either one or four (different) males. However, by sterilizing three of the four males with ionizing radiation, we eliminated any chance of sexual selection (in the polyandrous treatment) so that any differences in the female mating regimes must have been owing to maternal effects. Polyandry had no significant effect on daughter fecundity, thus indicating that any previously documented effects must have been genetic. This was further supported by a significant association between fathers' offensive sperm-competitive ability and the fecundity of their daughters. The association with fathers' sperm defensive ability was not significant, and neither was the association between fathers' sperm competitiveness and sons' reproductive success. However, sons of polyandrous females had lower reproductive success than sons of monandrous females. This shows that the maternal effects of polyandry should be taken into account whenever its costs and benefits are being considered.     

Evolutionary quantitative genetics of behavioral responses to handling in a wild passerine

Behavioral differences between individuals that are consistent over time characterize animal personality. The existence of such consistency contrasts to the expectation based on classical behavioral theory that facultative behavior maximizes individual fitness. Here, we study two personality traits (aggression and breath rate during handling) in a wild population of blue tits during 2007–2012. Handling aggression and breath rate were moderately heritable (h² = 0.35 and 0.20, respectively) and not genetically correlated (r_A = 0.06) in adult blue tits, which permits them to evolve independently. Reciprocal cross‐fostering (2007–2010) showed that offspring reared by more aggressive males have a higher probability to recruit. In addition, offspring reared by pairs mated assortatively for handling aggression had a higher recruitment probability, which is the first evidence that both parents' personalities influence their reproductive success in the wild in a manner independent of their genetic effects. Handling aggression was not subjected to survival selection in either sex, but slow‐breathing females had a higher annual probability of survival as revealed by capture–mark–recapture analysis. We find no evidence for temporal fluctuations in selection, and thus conclude that directional selection (via different fitness components) acts on these two heritable personality traits. Our findings show that blue tit personality has predictable fitness consequences, but that facultative adjustment of an individual's personality to match the fitness maximum is likely constrained by the genetic architecture of personality. In the face of directional selection, the presence of heritable variation in personality suggests the existence of a trade‐off that we have not identified yet.