Genetic variation in male effects on female reproduction and the genetic covariance between the sexes

Abstract.— Males of many insect species increase the fecundity and/or egg size of their mates through the amount or composition of their nuptial gifts or ejaculate. The genetic bases of such male effects on fecundity or egg size are generally unknown, and thus their ability to evolve remains speculative. Likewise, the genetic relationship between male and female investment into reproduction in dioecious species, which is expected to be positive if effects on fecundity are controlled by at least some of the same genes in males and females, is also unknown. Males of the seed beetle Stator limbatus contribute large ejaculates to females during mating, and the amount of donated ejaculate is positively correlated with male body mass. Females mated to large males lay more eggs in their lifetime than females mated to small males. We describe an experiment in which we quantify genetic variation in the number of eggs sired by males (mated to a single female) and found that a significant proportion of the phenotypic variance in the number of eggs sired by males was explained by their genotype. Additionally, the number of eggs sired by a male was highly positively genetically correlated with his body mass. The between-sex genetic correlation, that is, the genetic correlation between the number of eggs sired by males and the number of eggs laid by females, was highly positive when eggs were laid on Acacia greggii seeds. This indicates that males that sire many eggs have sisters that lay many eggs. Thus, some of the genes that control male ejaculate size (or some other fecundity-enhancing factor) when expressed in males appear to control fecundity when expressed in females. We found no significant interaction between male and female genotype on fecundity.     

Evolution under relaxed sexual conflict in the bulb mite Rhizoglyphus robini

The experimental evolution under different levels of sexual conflict have been used to demonstrate antagonistic coevolution in muscids, but among other taxa a similar approach has not been employed. Here, we describe the results of 37 generations of evolution under either experimentally enforced monogamy or polygamy in the bulb mite Rhizoglyphus robini. Three replicates were maintained for each treatment. Monogamy makes male and female interests congruent; thus selection is expected to decrease harmfulness of males to their partners. Our results were consistent with this prediction in that females from monogamous lines achieved lower fecundity when housed with males from polygamous lines. Fecundity of polygamous females was not affected by mating system under which their partners evolved, which suggests that they were more resistant to male-induced harm. As predicted by the antagonistic coevolution hypothesis, the decrease in harmfulness of monogamous males was accompanied by a decline in reproductive competitiveness. In contrast, female fecundity and embryonic viability, which were not expected to be correlated with male harmfulness, did not differ between monogamous and polygamous lines. None of the fitness components assayed differed between individuals obtained from crosses between parents from the same line and those obtained from crosses between parents from different lines within the same mating system. This indicates that inbreeding depression did not confound our results. However, interpretation of our results is complicated by the fact that both males and females from monogamous lines evolved smaller body size compared to individuals from polygamous lines. Although a decrease in reproductive performance of males from monogamous lines was still significant when body size was taken into account, we were not able to separate the effects of male body size and mating system in their influence on fecundity of their female partners.     

The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster

We studied two components of the mating system, copulation duration and early fecundity, in relation to body size in Drosophila melanogaster. Body size variation was created experimentally by varying the degree of crowding (starvation) among larvae from an inbred strain, keeping the genetics and temperature as constant as possible. Hence, in contrast to most previous studies, where genetic and environmental variation have been confounded, we aimed at investigating how much pure phenotypic variation could influence copulation duration and early fecundity. It is shown that copulation duration and fecundity both strongly dependent on female body size, but either not or much less so on male body size. Small females mate faster than medium or large females and small females have the lowest fecundity. Among males, medium-size males are more fecund than smaller or larger males, resulting in stabilising selection for intermediate male size. These results are in contrast with previous findings.     

Sexual dimorphism inAnastrepha suspensa (Loew) and other tephritid fruit flies (Diptera: Tephritidae): Possible roles of developmental rate,fecundity, and dispersal

Larger male Caribbean fruit flies are more likely to be chosen as mates and defeat rivals in territorial contests. Yet males are smaller than females. Adaptive explanations for relatively small male size include (1) acceleration of male development to maximize female encounter rates, (2) selection for greater female size to increase fecundity, and (3) selection for body sizes most suitable for sexually dimorphic degrees of mobility, speed, and distance flight. None of these unambiguously accounts for the degree of sexual dimorphism. Male development is not accelerated relative to that of females. On average, males remain inside fruit longer than females and those males with extended development periods are smaller than more rapidly developing individuals. There is no evidence that female enlargement alone, presumably for greater fecundity, has generated the degree of dimorphism in the Caribbean fruit fly or other fruit flies. The relationship between dimorphism and mean female body size in 27 species of Tephritidae is the opposite of what would be predicted if differences in dimorphism were due to differences in unilateral female enlargement. Larger size in a species or in one sex of a species may be an adaptation for extensive flight. In general, among 32 species of fruit flies, as body size increases, wing shape becomes progressively more suited for distance flight. However, there are important exceptions to this correlation. Both sexual selection and nonadaptive allometries may contribute to the range of dimorphisms within the family.     

Asymmetric size effect of sexes on reproductive fitness in an aphid parasitoid Aphidius ervi (Hymenoptera: Aphidiidae)

Most studies on size–fitness relationships focus on females and neglect males. Here, we investigated how body size of both sexes of an aphid parasitoid, Aphidius ervi Haliday, affected the reproductive fitness. Reproductive fitness was generally positively correlated with body size for both sexes in this species. Large individuals of both sexes had greater longevity, large males fathered more progeny, and large females had higher fecundity, parasitism, and greater ability in host searching and handling. We demonstrated in this study that size effects of males and females were asymmetric on different reproductive fitness parameters. With increasing body size females gained more than males in longevity and fecundity while males gained more than females in the number of female progeny. Regardless of female size, large males sustained a female-biased population longer than small males. These results suggest that male body size should also be considered in the quality control of mass-rearing programs and the evaluation of parasitoid population growth.     

Female cuticular hydrocarbons can signal indirect fecundity benefits in an insect

Male choosiness of prospective female mating partners provides an increasingly recognized pathway through which males can increase their fitness. For example, males may increase their number of offspring by targeting more fecund females as mating partners. If fecundity is heritable, males that mate with more fecund females can also receive the indirect benefit of more fecund daughters. In species where female fecundity is not directly assessable, female ornaments may act as signals of fecundity. However, whether female ornaments reliably signal the indirect benefit of more fecund daughters is not well understood. We investigated this question using the field cricket, Teleogryllus oceanicus. Previous work had identified the cuticular hydrocarbon (CHC) profile as a female sexual display trait in T. oceanicus. To examine whether CHCs can provide a reliable signal of fecundity, we tested whether individual CHC compounds and the first principal axis of CHC variation (PC1) are genetically correlated with ovary mass, a reliable proxy for fecundity in this species. We found significant genetic correlations between ovary mass and three individual CHC compounds, as well as PC1. This result indicates that by targeting females as mating partners based on their CHC profile, males can sire more fecund daughters.     

MALE EFFECTS ON FECUNDITY IN DROSOPHILA MELANOGASTER

Effects of male Drosophila melanogaster on female fecundity and productivity were examined, considering both females held in containers with males and females exposed to male effects not involving contact. Females were more fecund when male effects were present, and the largest increase was recorded when vials were previously conditioned by males. This effect was probably due to the growth of transmitted microorganisms, which were observed on the laying surface, as further experiments with vials conditioned by virgin females showed a similar increase in fecundity. A male-specific effect was isolated by conditioning bottles containing only agar with males and virgin females. The observation of a male factor that stimulates oviposition without mating is novel and suggests complicated fertility interactions between the sexes.     

Female masculinization and reproductive life history in the western mosquitofish (<Emphasis Type="Italic">Gambusia affinis</Emphasis>)

In this study, we explored the relationship between female masculinization and various morphological and reproductive parameters of male and female western mosquitofish (Gambusia affinis), including body size, anal fin length, testes mass and female fecundity. We detected high levels of female masculinization in the Brazos and Little Brazos Rivers (Falls County, Texas) in March 2008, but not 2009. In both populations, masculinized females were smaller, possessed shorter anal fins, and had significantly lower total fecundity (collective number of eggs and embryos) compared to non-masculinized females. In addition, 2008 non-masculinized females were smaller and less fecund than 2009 non-masculinized females in both populations. Moreover, 2008 males were smaller, had shorter gonopodia, and smaller testes than 2009 males. Our results support the hypothesis that female masculinization can have a strong influence on reproductive life history and population dynamics of livebearing fishes.     

Size Dependent Sexual Selection in Drosophila ananassae

Mate choice based on body size is widespread and can have numerous consequences. We present data, which show the effect of male and female body size on sexual selection in Drosophila ananassae. The relationships between wing size, locomotor activity, mating latency, courtship pattern, fertility and mating success were studied. Mating latency was negatively correlated with wing length and with locomotor activity, while wing length and locomotor activity was positively correlated in males as well as in females. In female- and male-choice, we found that mate choice influenced size-assortative mating by: (1) large and small males preferring to mate with large females, (2) large males successfully competing for large females, leaving small males to mate with small females. Males increased their reproductive success by mating with large and more fecund females. In addition, in pairs of long/short winged flies, long winged flies courted and mated more successfully than short winged flies and they also have longer duration of copulation and more progeny than short winged flies. We found sterile mating in pairs of small winged males and females.     

Ejaculate size, second male size, and moderate polyandry increase female fecundity in a seed beetle

Several hypotheses have been proposed to explain the evolutionof polyandry in species that provide nuptial gifts. When nuptialgifts are in the form of nutritional elements in the ejaculateand ejaculate size is correlated with male body size, femalescan accrue both direct (nutritional) and indirect (genetic)benefits from multiple mating. We examined remating decisionsin females of the seed beetle Stator limbatus and, using pathanalysis, examined the effects of male body size on the sizeof his ejaculate, the amount of ejaculate that was successfullytransferred to females, and the overall effect of these variableson female fecundity. Larger males produced larger ejaculatesand consequently transferred a larger ejaculate to females,but the effects on female fecundity differed between the females'first and second mates. Both larger first and second males wereable to transfer more of their ejaculate to females than weresmaller males. Both the total amount of ejaculate transferredby these males and polyandry (number of matings) were positivelycorrelated to female fecundity independently of each other.However, larger second males were more successful at stimulatingfemale fecundity independently of how much ejaculate they transferred.We also provide evidence that females are choosy during theirsecond mating opportunity. Both female choosiness and higherfemale investment after mating with larger second males suggestthat females may benefit from both direct and indirect effectsfrom multiple mating. We also conclude that male body size isunder both directional fecundity selection and directional sexualselection.     

Sex determination in the androdioecious plant Datisca glomerata and its dioecious sister species D. cannabina.

Datisca glomerata is an androdioecious plant species containing male and hermaphroditic individuals. Molecular markers and crossing data suggest that, in both D. glomerata and its dioecious sister species D. cannabina, sex is determined by a single nuclear locus, at which maleness is dominant. Supporting this conclusion, an amplified fragment length polymorphism (AFLP) is heterozygous in males and homozygous recessive in hermaphrodites in three populations of the androdioecious species. Additionally, hermaphrodite x male crosses produced 1:1 sex ratios, while hermaphrodite x hermaphrodite crosses produced almost entirely hermaphroditic offspring. No perfectly sex-linked marker was found in the dioecious species, but all markers associated with sex mapped to a single linkage group and were heterozygous in the male parent. There was no sex-ratio heterogeneity among crosses within D. cannabina collections, but males from one collection produced highly biased sex ratios (94% females), suggesting that there may be sex-linked meiotic drive or a cytoplasmic sex-ratio factor. Interspecific crosses produced only male and female offspring, but no hermaphrodites, suggesting that hermaphroditism is recessive to femaleness. This comparative approach suggests that the hermaphrodite form arose in a dioecious population from a recessive mutation that allowed females to produce pollen.     

Remating Behavior of Cnephasia jactatana Walker Females (Lepidoptera: Tortricidae)

Cnephasia jactatana Walker is an important pest of kiwifruit in New Zealand. We investigated, under laboratory conditions, the effects of multiple mating on the reproductive performance of C. jactatana females and how such effects varied with male virginity and larval nutrition. We found that in permanent pairs, remating increased female fecundity and fertility but suboptimally fed females benefited more from remating. Regardless of this benefit, mass-reared pairs had a lower remating frequency. Females remating with a virgin male or a male that had delivered a spermatophore presented similar fecundity and fertility; however, females receiving a second ejaculate from a virgin male had increased daily fecundity. Female weight clearly affected remating behavior since those that received a second ejaculate were significantly heavier. Neither mating length nor size of the first spermatophore influenced female remating. Further, mass-reared and individually reared males produced spermatophores of similar size.     

Female crickets trade offspring viability for fecundity

A growing number of studies are suggesting that females can improve the viability of their embryos by mating with multiple males. However, the reason why females should have low rates of embryo viability is puzzling. Here we conduct a quantitative genetic study of maternal effects on embryo viability in the field cricket Teleogryllus oceanicus. After controlling for female body size, we find significant additive genetic variance for ovary weight, a measure of fecundity, and egg hatching success, a measure of embryo viability. Moreover, we show a genetic trade-off between these traits that is predicted from life-history theory. High rates of embryo mortality in this highly fecund species might therefore be explained by selection favouring an optimum balance between fecundity and embryo viability that maximizes maternal fitness. Paternal effects on female fecundity and embryo viability are often seen as benefits driving the evolution of polyandrous behaviour. However, we raise the alternative possibility that paternal effects might shift females from their naturally selected optimum, and present some support for the notion that sexual conflict over a female's optimal fecundity and embryo viability might generate antagonistic coevolution between the sexes.     

Heteropopulation males have a fertilization advantage during sperm competition in the yellow dung fly (Scathophaga stercoraria)

Sexual conflict occurs whenever there is not strict genetic monogamy. The sexually antagonistic coevolution that potentially occurs because of this conflict involves adaptation by one sex followed by the counter-adaptation by the other, and may be thought of as an evolutionary arms-race. As a result of these cycles of antagonistic coevolution, females from one population may be less resistant to heteropopulation males, at least after short periods of allopatry, as they will not have evolved any resistance to them. We tested this prediction in yellow dung fly (Scathophaga stercoraria) populations from the UK and Switzerland. Males from each population mated as first and second males to females from each population, and the mean numbers of offspring sired by the last male to mate in each situation were compared. We also compared the fertility and fecundity of single females mated to males from both populations, as well as the fertility and fecundity of the F(1) crosses. Both crosses produced viable and fertile offspring and the offspring sex ratios were not skewed. However, the fecundity of F(1)-cross females was greater than that of the parentals. In the sperm-competition experiment, there was a significant interaction between male and female origin influencing the proportion of offspring sired by the second male to mate, with heteropopulation males always outcompeting conpopulation males. This effect was independent of copula duration and the delay between copulations. In a separate experiment, we tested to see whether this was due to female preference for genetically dissimilar males but found no evidence for paternity biasing based on genetic similarity. Our results therefore seem to be best explained by sexually antagonistic coevolution as females appear less resistant to males with which they have not coevolved.     

The effect of 2n gametes on sex ratios in Actinidia

Sex can sometimes lead to complications. In some crops, 2n gametes have been exploited by plant breeders to transfer genetic variation between taxa of different ploidy levels. However, their role and use in dioecious genera have received relatively little attention. In the dioecious genus Actinidia (kiwifruit), seedling populations usually segregate equally for females and males as sex is determined by an XX female/XY male system. While fertilization involving 2n egg cells is not expected to affect the sex ratios of progenies, fertilization involving 2n pollen is likely to produce progenies with excess males. The extent of sex ratio distortion will depend on the relative contributions of first and second division restitution, and the frequency and location of cross-overs in meiosis. In this study, seedlings recovered from crosses between females of hexaploid Actinidia deliciosa and males of two diploid species, Actinidia chinensis and Actinidia eriantha, included a proportion of pentaploid hybrids presumably derived from fertilization involving 2n pollen. Most of these pentaploids were male, and a proportion of them were likely to be carrying two Y chromosomes. If used as parents in further crosses, males with multiple Y chromosomes are likely to cause distorted sex ratios in their immediate progenies. In dioecious genera such as Actinidia, the effects on sex ratios of different mechanisms of ploidy change need to be taken into account when considering the evolution of polyploidy and the design of breeding strategies involving ploidy manipulation.     

Animal dispersal dynamics promoting dioecy over hermaphroditism

Because of the separation of sexual function to male and female individuals, dioecious species have fewer pollen and seed bearers and thus experience disadvantages due to increased aggregation of reproductive function. Because of this disadvantage, models predict that dioecious females must have substantially more than twice the fecundity of hermaphrodites, yet empirical data suggest that female fecundity advantages are commonly much lower. Here, we incorporate animal foraging dynamics--and the heightened dispersal of seeds that may accompany increases in fecundity of dioecious females--into a spatially explicit mathematical model. We focus on the competition for germination sites with varying seed production, seed dispersal ability, and mortality, and we find that preferential foraging on dioecious females reduces the stringent fecundity requirements of dioecy to values in accordance with empirical estimates. This finding contributes to our understanding of the correlation between dioecy and fleshy fruits and highlights the importance of mutualist dispersers to dioecious species.     

Mate choice by males of the hermit crab Pagurus filholi: Do males assess ripeness and/or fecundity of females?

Males of the hermit crab, Pagurusfilholi, often grasp the edges of shells occupied by females and drag them during the mating season. This behavior was experimentally confirmed to be a precopulatory guarding behavior displayed by males for ripe females, and males were found to recognize females which were within about 5 days of spawning. Most theoretical models for mating preference assume the choosing sex (the male in the present case) has complete reproductive information about potential mates, and predict that males will preferably choose more fecund females and/or females that will require less guarding time (i.e. that will spawn sooner) as partners. Several male-choice experiments between two ripe females, both previously guarded by other males, were carried out to examine the above predictions. Males did not prefer females of larger size, higher fecundity or with less time remaining until spawning. These results suggest that males may not have complete information about potential partners, rather that male hermit crabs may adopt a mating strategy of pairing with the first ripe female they encounter. Even with such incomplete mate assessment, males may enhance their reproductive success by recognizing ripe females that will spawn within a given time (about 5 days in the present case).     

Ejaculate investment and attractiveness in the stalk‐eyed fly,Diasemopsis meigenii

The phenotype‐linked fertility hypothesis proposes that male fertility is advertised via phenotypic signals, explaining female preference for highly sexually ornamented males. An alternative view is that highly attractive males constrain their ejaculate allocation per mating so as to participate in a greater number of matings. Males are also expected to bias their ejaculate allocation to the most fecund females. We test these hypotheses in the African stalk‐eyed fly, Diasemopsis meigenii. We ask how male ejaculate allocation strategy is influenced by male eyespan and female size. Despite large eyespan males having larger internal reproductive organs, we found no association between male eyespan and spermatophore size or sperm number, lending no support to the phenotype‐linked fertility hypothesis. However, males mated for longer and transferred more sperm to large females. As female size was positively correlated with fecundity, this suggests that males gain a selective advantage by investing more in large females. Given these findings, we consider how female mate preference for large male eyespan can be adaptive despite the lack of obvious direct benefits.     

Mate choice by male water striders (Gerris lacustris): expression of a wing morph preference depends on a size difference between females

Natural selection maintains wing polymorphism in populationsof water striders. Long-winged females benefit from being ableto migrate because they avoid the risk of pool evaporation,but early in the season their fecundity is lower than that ofshort-winged females. We tested preferences of 18 long-wingedmales and 29 short-winged males in spring. Males preferred long-wingedfemales, and there was no difference between the two male morphs.The preference was only observed when the long-winged femalewas heavier; when the short-winged female was larger, the malesshowed no preference. There was a positive relationship betweenlong-winged female weight and number of eggs laid per day, andthe males behaved as if they were taking into account that large,long-winged females are more fecund. We suggest that males preferredlong-winged females because this preference increases the proportionof long-winged individuals in the autumn F2 generation.     

Complex sex determination in the stinging nettle Urtica dioica

The dioecious species Urtica dioica harbours wide variation in sex ratio of seeds. We conducted a series of crosses to analyse the genetic basis of sex determination in this species. Dutch populations of U. dioica contain low proportions of monoecious individuals beside male and female plants. Self-pollination of monoecious plants always yielded female, male and monoecious plants, generally in a ratio of one female to three male/monoecious individuals. This motivated us to write down a simple model in which gender is determined by one major sex-determination locus with four alleles. In the model males and monoecious plants have distinct genotypes but are both heterozygous at the sex-determination locus. We first made crosses among progeny obtained after self-pollination of monoecious plants. These crosses showed that the monoecious trait generally showed Mendelian inheritance and was passed on to the next generation via both pollen and seeds. Further crosses between monoecious plants and plants from dioecious system indicated that alleles from the dioecious system are often dominant. However, many exceptions to our genetic model are observed which suggest that dominance is incomplete and/or that more genes are involved in sex determination. We discuss to what extent sex determination genes explain the strongly biased seed sex ratios and argue that additional genes, for instance genes for female choice, must also be involved.