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The evolution of polyandry (female multiple mating)

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Shorter sperm confer higher competitive fertilization success
Garcia-Gonzalez, F. & Simmons, L. W. 2007 Shorter sperm confer higher competitive fertilization success Evolution, 61: 816-824

Spermatozoa exhibit taxonomically widespread patterns of divergent morphological evolution. However, the adaptive significance of variation in sperm morphology remains unclear. In this study we examine the role of natural variation in sperm length on fertilization success in the dung beetle Onthophagus taurus. We conducted sperm competition trials between males that differed in the length of their sperm and determined the paternity of resulting offspring using amplified fragment length polymorphism (AFLP) markers. We also quantified variation in the size and shape of the female’s sperm storage organ to determine whether female morphology influenced the competitiveness of different sperm morphologies. We found that fertilization success was biased toward males with relatively shorter sperm, but that selection on sperm length was dependent on female tract morphology; selection was directional for reduced sperm length across most of the spermathecal size range, but stabilizing in females with the smallest spermathecae. Our data provide empirical support for the theory that sperm competition should favor the evolution of numerous tiny sperm. Moreover, because sperm length is both heritable and genetically correlated with condition, our results are consistent with a process by which females can accrue genetic benefits for their offspring from the incitement of sperm competition and/or cryptic female choice, as proposed by the “sexy sperm” and “good sperm” models for the evolution of polyandry.

Female crickets trade offspring viability for fecundity
Simmons, L. W. & Garcia-Gonzalez, F. 2007 Female crickets trade offspring viability for fecundity Journal of Evolutionary Biology, 20: 1617-1623
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.
Sources of genetic and phenotypic variance in sperm performance and larval traits in a sea urchin
Evans, J. P., Garcia-Gonzalez, F. & Marshall, D. J. 2007 Sources of genetic and phenotypic variance in sperm performance and larval traits in a sea urchin Evolution, 61: 2832-2838
In nonresource based mating systems females are thought to derive indirect genetic benefits by mating with high-quality males. Such benefits can be due either to the intrinsic genetic quality of sires or to beneficial interactions between maternal and paternal haplotypes. Animals with external fertilization and no parental care offer unrivaled opportunities to address these hypotheses. With these systems, cross-classified breeding designs and in vitro fertilization can be used to disentangle sources of genetic and environmental variance in offspring fitness. Here, we employ these approaches in the Australian sea urchin Heliocidaris erythrogramma and explore how sire–dam identities influence fertilization rates, embryo viability (survival to hatching), and metamorphosis, as well as the interrelationships between these potential fitness traits. We show that fertilization is influenced by a combination of strong maternal effects and intrinsic male effects. Our subsequent analysis of embryo viability, however, revealed a highly significant interaction between parental genotypes, indicating that partial incompatibilities can severely limit offspring survival at this life-history stage. Importantly, we detected no significant relationship between fertilization rates and embryo viability. This finding suggests that fertilization rates should not be inferred from hatching rates, which is commonly practiced in species in which it is not possible to estimate fertilization at conception. Finally, we detected significant additive genetic variance due to sires in rates of juvenile metamorphosis, and a positive correlation between fertilization rates and metamorphosis. This latter finding indicates that the performance of a male’s ejaculate in noncompetitive IVF trials predicts heritable offspring traits, although the fitness implications of variance in rates of spontaneous juvenile metamorphosis have yet to be determined.
The evolution of polyandry: intrinsic sire effects contribute to embryo viability
Garcia-Gonzalez, F. & Simmons, L. W. 2005 The evolution of polyandry: intrinsic sire effects contribute to embryo viability Journal of Evolutionary Biology, 18:1097-1103
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.
Sperm viability matters in insect sperm competition
Garcia-Gonzalez, F. & Simmons, L. W. 2005 Sperm viability matters in insect sperm competition Current Biology, 15: 271-275

Female promiscuity often results in the ejaculates of different males competing to fertilize a female's ova. Experimental studies in insects have shown how sperm competition can be a potent selective force acting on an array of male reproductive traits, including features of the ejaculate such as sperm numbers or sperm size. However, experimental analysis of the role of sperm quality in determining paternity in insects has been neglected, despite the fact that sperm quality has been shown to influence the outcome of sperm competition in vertebrates. A recent comparative analysis found that males of polyandrous insect species show a higher proportion of live sperm in their stores, suggesting that sperm competition has shaped the quality of insect sperm. Here we test the hypothesis that sperm viability influences paternity at the within-species level. We use the cricket Teleogryllus oceanicus to conduct sperm competition trials involving pre-screened males that differ in the viability of their sperm. We find that paternity success is determined by the proportion of live sperm in a male's ejaculate. Furthermore, we were able to predict the patterns of paternity observed on the basis of the males' relative representation of viable sperm in the female's sperm storage organ. Our findings provide the first experimental evidence for the theory that sperm competition selects for higher sperm quality in insects, and indicate that between-male variation in sperm quality needs to be considered in theoretical and experimental studies of insect sperm competition.

Infertile matings and sperm competition: the effect of non sperm representation on intraspecific variation in sperm precedence patterns
Garcia-Gonzalez, F. 2004 Infertile matings and sperm competition: the effect of "non sperm representation" on intraspecific variation in sperm precedence patterns American Naturalist, 164: 457-472

In theoretical and experimental approaches to the study of sperm competition, it is often assumed that ejaculates always contain enough sperm of good quality and that they are successfully transferred and used for fertilization. However, this view neglects the potential effects of infertility and sperm limitation. Permanent or temporal male infertility due to male sterility, insemination failures, or failures to fertilize the ova implies that some males do not achieve sperm representation in the female reproductive tract after mating. A review of the literature suggests that rates of nonsperm representation may be high; values for the proportion of infertile matings across 30 insect species vary between 0% and 63%, with the median being 22%. I simulated P2 (the proportion of offspring fathered by the second male to copulate with a female in a double-mating trial) distributions under a mechanism of random sperm mixing when sample sizes and rates of male infertility varied. The results show that nonsperm representation can be responsible for high intraspecific variance in sperm precedence patterns and that it can generate misleading interpretations about the mechanism of sperm competition. Nonsperm representation might be a common obstacle in the studies of sperm competition and postcopulatory female choice.

Sperm competition mechanisms, confidence of paternity, and the evolution of paternal care in the golden egg bug (Phyllomorpha laciniata)
Garcia-Gonzalez, F., Núñez, Y., Ponz, F., Roldán, E. R. S., and Gomendio, M. 2003 Sperm competition mechanisms, confidence of paternity, and the evolution of paternal care in the golden egg bug (Phyllomorpha laciniata) Evolution, 57:1078-1088

Theoretical models predict how paternal effort should vary depending on confidence of paternity and on the trade-offs between present and future reproduction. In this study we examine patterns of sperm precedence in Phyllomorpha laciniata and how confidence of paternity influences the willingness of males to carry eggs. Female golden egg bugs show a flexible pattern of oviposition behavior, which results in some eggs being carried by adults (mainly males) and some being laid on plants, where mortality rates are very high. Adults are more vulnerable to predators when carrying eggs; thus, it has been suggested that males should only accept eggs if there are chances that at least some of the eggs will be their true genetic offspring. We determined the confidence of paternity for naturally occurring individuals and its variation with the time. Paternity of eggs fertilized by the last males to mate with females previously mated in the field has been determined using amplified fragment length polymorphisms (AFLPs). The exclusion probability was 98%, showing that AFLP markers are suitable for paternity assignment. Sperm mixing seems the most likely mechanism of sperm competition, because the last male to copulate with field females sires an average of 43% of the eggs laid during the next five days. More importantly, the proportion of eggs sired does not change significantly during that period. We argue that intermediate levels of paternity can select for paternal care in this system because: (1) benefits of care in terms of offspring survival are very high; (2) males have nothing to gain from decreasing their parental effort in a given reproductive event because sperm mixing makes it difficult for males to reach high paternity levels and males are left with no cues to assess paternity; (3) males cannot chose to care for their offspring exclusively because they can neither discriminate their own eggs, nor can they predict when their own eggs will be produced; and (4) males suffer no loss of further matings with other females when they carry eggs. Thus, our findings do not support the traditional view that paternal investment is expected to arise only in species where confidence of paternity is high. The results suggest that females maximize the chances that several males will accept eggs at different times by promoting a mechanism of sperm mixing that ensures that all males that have copulated with a female have some chance of fathering offspring, that this probability remains constant with time, and that males have no cues as to when their own offspring will be produced.

A field test of the intraspecific brood parasitism hypothesis in the golden egg bug (Phyllormorpha laciniata)
Garcia-Gonzalez, F. and Gomendio, M. 2003 A field test of the intraspecific brood parasitism hypothesis in the golden egg bug (Phyllormorpha laciniata) Behavioral Ecology and Sociobiology, 53:332-339

In natural populations of golden egg bugs (Phyllomorpha laciniata), females lay eggs on plants where they develop unattended, or on conspecifics, where they remain firmly glued until the nymphs hatch and start an independent life. Mortality rates among eggs laid on plants are higher than among eggs carried by adults. Because females cannot lay eggs on themselves, in order to improve offspring survival, they have to lay eggs on other individuals. Two hypotheses have been proposed to explain egg carrying: (1) the mating pair intraspecific brood parasitism hypothesis suggests that females dump eggs on copulating pairs, and (2) the paternal care hypothesis suggests that the system is driven mainly by males accepting eggs to improve the survival rates of their own offspring. Our data from the field show that 77% of the eggs are carried by males, because more males than females carry eggs, and because males carry a greater number of eggs. In addition, we show that mating males carry more recently laid eggs than single males. These results support the view that egg carrying is performed predominantly by males and that eggs are laid on males by their current mating partner, probably between repeated copulations. Males are likely to accept eggs, despite intermediate levels of paternity, because they cannot discriminate in favour of their own eggs, because rejected eggs will face 97% mortality rates on plants, and because they do not suffer mating costs when they carry eggs. However, females carry 23% of the eggs, but no differences in egg carrying have been found between mating and single females, suggesting that this is not the result of egg dumping while females are copulating. Egg carrying by females could reflect low levels of intraspecific parasitism, which is likely to reflect the low rate of successful attempts by egg-laying females who try to oviposit on other conspecifics rather indiscriminately, in an effort to improve the survival of their offspring.

Variation in paternity in the field cricket Teleogryllus oceanicus: no influence of sperm numbers or sperm length
Simmons, L.W.; Wernham, J.; Garcia-Gonzalez, F. & Kamien, D. 2002 Variation in paternity in the field cricket Teleogryllus oceanicus: no influence of sperm numbers or sperm length Behavioral Ecology, 14: 539-545
Recent attention has focused on the role that sperm competition may play in the evolution of sperm morphology. Theoretical analyses predict increased sperm size, decreased sperm size, and no change in sperm size in response to sperm competition, depending on the assumptions made concerning the life history and function of sperm. However, although there is good evidence that sperm morphology varies widely within and between species, the adaptive significance of this variation has not been examined. Here we document significant intraspecific variation in sperm length in the field cricket, Teleogryllus oceanicus. Sperm length did not influence the rate of migration of sperm from the spermatophore to the female’s spermatheca. We performed sperm competition trials in which we varied the numbers of sperm transferred by each of two males that differed in the length of sperm they produced. Neither sperm length nor the number of sperm transferred influenced paternity. The same results were obtained using two different methods for assigning paternity. The distribution of paternity across a female’s mates was highly variable, with frequently one, or more in the case of females mated to four males, principal sire. There were no mating order effects on paternity. These data show that sperm do not mix randomly in the female’s spermatheca. We discuss several alternative explanations for the patterns of paternity observed.
No evidence for heritability of male mating latency or copulation duration across social environments in Drosophila melanogaster
Taylor, M. L., Evans, J. P. and Garcia-Gonzalez, F. 2013 No evidence for heritability of male mating latency or copulation duration across social environments in Drosophila melanogaster PLoS ONE, 8:e77347
A key assumption underpinning major models of sexual selection is the expectation that male sexual attractiveness is heritable. Surprisingly, however, empirical tests of this assumption are relatively scarce. Here we use a paternal fullsib/half-sib breeding design to examine genetic and environmental variation in male mating latency (a proxy for sexual attractiveness) and copulation duration in a natural population of Drosophila melanogaster. As our experimental design also involved the manipulation of the social environment within each full-sibling family, we were able to further test for the presence of genotype-by-environment interactions (GEIs) in these traits, which have the potential to compromise mate choice for genetic benefits. Our experimental manipulation of the social environment revealed plastic expression of both traits; males exposed to a rival male during the sensitive period of adult sexual maturation exhibited shorter mating latencies and longer copulation durations than those who matured in isolation. However, we found no evidence for GEIs, and no significant additive genetic variation underlying these traits in either environment. These results undermine the notion that the evolution of female choice rests on covariance between female preference and male displays, an expectation that underpins indirect benefit models such as the good genes and sexy sons hypotheses. However, our results may also indicate depletion of genetic variance in these traits in the natural population studied, thus supporting the expectation that traits closely aligned with reproductive fitness can exhibit low levels of additive genetic variance.