The potential for disruptive selection on growth rates across genetically influenced alternative reproductive tactics

A trade-off between survival to sexual maturity and mating success is common across alternative reproductive tactics (ARTs), and can lead to tactical disruptive selection on shared traits (i.e. positive selection gradient in one tactic, and negative selection gradient in another). We were interested in examining the theoretical possibility of tactical disruptive selection on intrinsic growth rate. The male ARTs in Xiphophorus multilineatus express two distinct life histories: “courters” optimize mating success by maturing later at larger size and coaxing females to mate, while “sneakers” optimize survival to sexual maturity by maturing earlier at a smaller size, using both coaxing and coercive mating behaviors. In addition to differences in mating behaviors, body length, body depth, and the pigment pattern vertical bars, courter males grow faster than sneaker males. We present a new hypothesis for differences in growth rates between genetically influenced ARTs. The “growth-maturity optimization” hypothesis suggests that ARTs with differences in the probability of surviving to sexual maturity may have different optimal growth rates, leading to tactical disruptive selection. We also present a simple model to suggest that when considering both a cost and benefit to faster growth, tactical disruptive selection on growth rates is theoretically possible. In our model, the value that determines when tactical disruptive selection on growth rate will occur is the increase in probability of survival to sexual maturity gained through faster growth multiplied by the cost of faster growth (reduced longevity). Finally, we present empirical evidence to support the prediction that faster growth has a cost in X. multilineatus: in a controlled laboratory setting, courter males that did not survive 1.2 years past sexual maturity grew faster as juveniles (14–70 days) than those that survived.     

Maternal effects are long‐lasting and influence female offspring's reproductive strategy in the swordtail fish Xiphophorus multilineatus

The adaptive benefits of maternal investment into individual offspring (inherited environmental effects) will be shaped by selection on mothers as well as their offspring, often across variable environments. We examined how a mother's nutritional environment interacted with her offspring's nutritional and social environment in Xiphophorus multilineatus, a live‐bearing fish. Fry from mothers reared on two different nutritional diets (HQ = high quality and LQ = low quality) were all reared on a LQ diet in addition to being split between two social treatments: exposed to a large adult male during development and not exposed. Mothers raised on a HQ diet produce offspring that were not only initially larger (at 14 days of age), but grew faster, and were larger at sexual maturity. Male offspring from mothers raised on both diets responded to the exposure to courter males by growing faster; however, the response of their sisters varied with mother's diet; females from HQ diet mothers reduced growth if exposed to a courter male, whereas females from LQ diet mothers increased growth. Therefore, we detected variation in maternal investment depending on female size and diet, and the effects of this variation on offspring were long‐lasting and sex specific. Our results support the maternal stress hypothesis, with selection on mothers to reduce investment in low‐quality environments. In addition, the interaction we detected between the mother's nutritional environment and the female offspring's social environment suggests that female offspring adopted different reproductive strategies depending on maternal investment.     

Experimental manipulation of female tail length did not cause differential allocation by males in the barn swallow

The evolution and maintenance of female ornamentation has attracted increasing attention, because the previous explanation, that is a non‐functional copy of functional male ornamentation, seems insufficient to explain female ornamentation. A post‐mating sexual selection, differential allocation, may be more common than pre‐mating sexual selection, but few studies have investigated differential allocation by males. Here, we studied differential allocation of incubation investment by male barn swallows Hirundo rustica, a model species for the study of sexual selection, because our previous correlative study demonstrated a positive relationship between female tail length and male incubation investment. We manipulated the length of the outermost tail feathers in females after clutch completion and examined whether males adjust incubation investment according to female ornamentation. Because extra‐pair paternity is virtually absent in the study population, we were able to study differential allocation based on the tradeoff between current and future reproductive investments, rather than the tradeoff between current paternal investment and additional mating effort. The experimental treatment had no significant effect on male nest attentiveness, whereas female tail length before manipulation predicted male nest attentiveness. The observed pattern is consistent with differential access; that is, well‐ornamented individuals have greater access to mates with high reproductive (parental) ability, rather than differential allocation during incubation. Alternatively, males can directly assess eggs in their nests, and thus, as seen in other species, males might adjust their incubation investment based on the egg characteristics of long‐tailed females.     

Offspring sex ratio produced by female guppies in the wild correlates with sexual ornaments of their sons

The attractiveness hypothesis predicts that females produce broods with male-biased sex ratios when they mate with attractive males. This hypothesis presumes that sons in broods with male-biased sex ratios sired by attractive males have high reproductive success, whereas the reproductive success of daughters is relatively constant, regardless of the attractiveness of their sires. However, there is little direct evidence for this assumption. We have examined the relationships between offspring sex ratios and (1) sexual ornamentation of sons and (2) body size of daughters in broods from wild female guppies Poecilia reticulata. Wild pregnant females were collected and allowed to give birth in the laboratory. Body size and sexual ornamentation of offspring were measured at maturity. Our analysis revealed a significant positive correlation between offspring sex ratios (the proportion of sons per brood) and the total length as well as the area of orange spots of sons, two attributes that influence female mating preferences in guppies. The sex ratio was not associated with the body size of daughters. These results suggest that by performing adaptive sex allocation according to the expected reproductive success of sons and daughters, female guppies can enhance the overall fitness of their offspring.     

Male dominance determines female egg laying rate in crickets

A key prediction of theories of differential allocation and sexual conflict is that male phenotype will affect resource allocation by females. Females may adaptively increase investment in offspring when mated to high quality males to enhance the quality of their offspring, or males may vary in their ability to manipulate female investment post-mating. Males are known to be able to influence female reproductive investment, but the male traits underlying this ability have been little studied in taxa other than birds. We investigated the relationship between male dominance and female oviposition rate in two separate experiments using the field cricket, Gryllus bimaculatus. In both experiments, females mated to more dominant (but not larger) males laid more eggs. This reveals that either females allocate more effort to reproduction after mating with a dominant male or that dominance status is associated with male ability to manipulate their mates. This is the first evidence that dominance, rather than male attractiveness, has a post-copulatory effect on reproductive investment by females.     

Differential allocation in a lekking bird: females lay larger eggs and are more likely to have male chicks when they mate with less related males

The differential allocation hypothesis predicts increased investment in offspring when females mate with high-quality males. Few studies have tested whether investment varies with mate relatedness, despite evidence that non-additive gene action influences mate and offspring genetic quality. We tested whether female lekking lance-tailed manakins (Chiroxiphia lanceolata) adjust offspring sex and egg volume in response to mate attractiveness (annual reproductive success, ARS), heterozygosity and relatedness. Across 968 offspring, the probability of being male decreased with increasing parental relatedness but not father ARS or heterozygosity. This correlation tended to diminish with increasing lay-date. Across 162 offspring, egg volume correlated negatively with parental relatedness and varied with lay-date, but was unrelated to father ARS or heterozygosity. Offspring sex and egg size were unrelated to maternal age. Comparisons of maternal half-siblings in broods with no mortality produced similar results, indicating differential allocation rather than covariation between female quality and relatedness or sex-specific inbreeding depression in survival. As males suffer greater inbreeding depression, overproducing females after mating with related males may reduce fitness costs of inbreeding in a system with no inbreeding avoidance, while biasing the sex of outbred offspring towards males may maximize fitness via increased mating success of outbred sons.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem‐defending arachnid

When there is a temporal trade‐off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high‐quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low‐quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males’ decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem‐holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade‐off between mating effort and parental care is circumvented.     

Offspring sex ratio allocation in the parasitic jaeger: selection for pale females and melanic males?

The maintenance of plumage color polymorphism in the parasiticjaeger (Stercorarius parasiticus) is still not well understood.Earlier studies indicated that selection may favor pale femalesand melanic males. If so, females would maximize their fitness,producing pale female and melanic male offspring. We thereforepredicted that females might bias their offspring sex ratiotoward daughters in pale pairs and toward sons in melanic pairs.Females might also choose to mate assortatively in relationto plumage color, thereby maximizing the probability of producingeither pale or melanic offspring. Because females are largerthan males, differential rearing costs may affect the offspringsex ratio independent of parental plumage color. We examinedoffspring sex ratio allocation, breeding variables indicativeof parental quality, and mating pattern in relation to plumagecolor in a colony of parasitic jaegers in northern Norway. Jaegerstended to mate assortatively in relation to plumage color. Thereproductive performance declined with season, and matched pairsappeared to be of lower quality than mixed pairs. The proportionof male offspring increased with hatching date in matched paleand mixed pairs, whereas the situation was reversed in matchedmelanic pairs. Matched pale pairs produced an overall surplusof favorable pale but costly daughters despite their lower quality,while melanic pairs produced a surplus of favorable melanicsons. However, differential offspring rearing costs and parentalrearing capacity may have additionally affected the realizedoffspring sex ratio. Mixed pairs producing an overall surplusof pale and melanic daughters allocated their resources accordingto differential rearing costs and parental quality only. Wesuggest that both strategies of sex ratio allocation togetherwith differences in reproductive success in matched versus mixedpairs may have a balancing effect on the mating pattern betweenplumage morphs and may contribute to the maintenance of thecolor polymorphism in this species.     

INBREEDING DEPRESSION VARIES WITH INVESTMENT IN SEX IN A FACULTATIVE PARTHENOGEN

The reproductive mode of facultative parthenogens allows recessive mutations that accumulate during the asexual phase to be unmasked following sexual reproduction. Longer periods of asexual reproduction should increase the accumulation of deleterious mutations within individuals, reduce population-level genetic diversity via competition and increase the probability of mating among close relatives. Having documented that the investment in sexual reproduction differs among populations and clones of Daphnia pulicaria , we ask if this variation is predictive of the level of inbreeding depression across populations. In four lake populations that vary in sex investment, we raised multiple families (mother, field-produced daughter, laboratory-produced daughter) on high food and estimated the fitness reduction in both sexually produced offspring relative to the maternal genotype. Inbred individuals had lower fitness than their field-produced siblings. The magnitude of fitness reduction in inbred offspring increased as population-level investment in sex decreased. However, there was less of a fitness reduction following sex in the field-produced daughters, suggesting that many field-collected mothers were involved in outcross mating.     

Sex differences in begging vocalizations of nestling barn swallows, Hirundo rustica

Parents of sexually reproducing species should adjust their investment in production of sons and daughters in relation to the relative costs and reproductive value of offspring of either sex. Sex allocation mediated by differential allocation of care such as food provisioning, however, requires that parents can identify offspring sex. We analysed sex differences in offspring begging calls that may serve as a cue for parents to discriminate between sons and daughters. A combination of three sonagraphic variables of begging calls of nestling barn swallows allowed us to classify them according to sex at day 16, but not at day 12 after hatching, suggesting that sex differences in begging calls arise during the nestling period as the time of fledging approaches. Hence, parents may be able to discriminate between sons and daughters by auditory cues, which would enable differential allocation of food between offspring during the late nestling and early fledging stages. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Effects of the juvenile hormone analogue methoprene and dietary protein on male melon fly Bactrocera cucurbitae (Diptera: Tephritidae) mating success

The effect of access to dietary protein (P) and the topical application of a juvenile hormone analogue (methoprene (M)) on mating behaviour of male melon fly Bactrocera cucurbitae was assessed in the laboratory and in field cages. Age, dietary protein and methoprene application increased the mating success and influenced the mating behaviour. Treatment with methoprene (M+) to protein-deprived (P−) males had only a modest effect on the acceleration of sexual maturity, but application of methoprene (M+) to protein-fed (P+) males greatly accelerated sexual maturity. Protein diet (P+) increased mating success of males in comparison to protein-deprived (P−) males. Protein and methoprene have a synergistic effect on mating behaviour, since M + P+ treated males exhibit reduced mating latency and achieved higher mating in younger ages than methoprene and/or protein-deprived males. Copulation duration was correlated with nutritional status and M + P+ males copulated longer at the age of advanced sexual maturity than M − P+ males. Our results suggest that in this species with a lek mating system, females discriminate between the males based on their sexual signals, which were influenced by protein in the adult diet, methoprene application and age. The results are discussed in the light of mating competitiveness of precocious treated young males and their relevance to Sterile Insect Technique application against this pest species.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

Big mothers invest more in daughters – reversed sex allocation in a weakly polygynous mammal

How mothers allocate resources to offspring is central to understanding life history strategies. High quality mothers are predicted to favour investment in sons over daughters when to do so increases inclusive fitness. This is the case in ungulates with polygynous mating systems, where reproductive success is more variable among males than females, but information is scarce on sex allocation in less polygynous species. Here, for the weakly dimorphic roe deer, we show that as maternal capacity to invest increases, mothers increase allocation to daughters more than to sons, so that relative allocation to daughters increases markedly with increasing maternal quality. This cannot be explained by a between sex difference in growth priority, hence we conclude that this is evidence for active maternal discrimination. Further, we demonstrate that condition differences between offspring persist to adulthood. For high quality mothers of weakly polygynous species, daughters may be more valuable than sons.     

Predator-induced maternal and paternal effects independently alter sexual selection

Parental experience alters survival-related phenotypes of offspring in both adaptive and nonadaptive ways, yielding rapid inter- and transgenerational fitness effects. Yet, fitness comprises survival and reproduction, and parental effects on mating decisions could alter the strength and direction of sexual selection, affecting long-term evolutionary trajectories. We used a full factorial design in which threespine stickleback (Gasterosteus aculeatus) mothers, fathers, both, or neither were exposed to a model predator at developmentally appropriate times to test for predator-induced maternal, paternal, and joint parental effects on daughters’ mating behavior. We tested the responsiveness, preferences, and mate choices of adult daughters in no-choice trials with wild-caught males who had varied sexual signals. Maternal and paternal predator exposure independently yielded daughters who preferred males who were intermediate in conspicuousness (with duller nuptial coloration and who courted less vigorously), relaxing the typical preference for the most conspicuous males. The combined effects of maternal and paternal predator exposure were not cumulative; when both parents were predator exposed, single-parent effects on mate preferences were reversed. Thus, we cannot assume that maternal and paternal effects additively combine to produce “parental” effects. Further, joint parental predator exposure yielded daughters who were three times less likely to mate at all. Stress-induced intergenerational parental effects on reproductive decisions such as those observed here may potentiate rapid transgenerational responses to novel and changing mating environments.     

Tradeoffs between growth and reproduction in response to temporal variation in food supply

Allocating resources to growth or to reproduction is a fundamental tradeoff in evolutionary life history theory. In environments with unpredictable food resources, natural selection is expected to favor increased allocation to reproduction. Although effects of selection are realized only across generations, short-term changes in food predictability might influence intra-generational tradeoffs in resource allocation. We assessed the ability of fathead minnows, Pimephales promelas, to adjust allocation to growth and reproduction in response to predictable, unpredictable, and switched feeding schedules. Fish in the switched treatments were changed from unpredictable to predictable feeding schedules just after reaching sexual maturity. Egg production did not differ significantly among treatments despite the fact that females on the unpredictable and switched feeding schedules grew more slowly than those on the predictable schedule. Switched males were heavier and had proportionally larger testes than males in predictable and unpredictable treatments. Increased allocation to reproduction or growth by fish on unpredictable and switched feeding schedules was associated with changes in gut length relative to body mass. Both sexes showed a remarkable degree of phenotypic plasticity in response to resource availability and sex differences in allocation patterns were consistent with adaptive responses in the context of the fathead mating system.     

Daphnia females adjust sex allocation in response to current sex ratio and density

Cyclical parthenogenesis presents an interesting challenge for the study of sex allocation, as individuals’ allocation decisions involve both the choice between sexual and asexual reproduction, and the choice between sons and daughters. Male production is therefore expected to depend on ecological and evolutionary drivers of overall investment in sex, and those influencing male reproductive value during sexual periods. We manipulated experimental populations, and made repeated observations of natural populations over their growing season, to disentangle effects of population density and the timing of sex from effects of adult sex ratio on sex allocation in cyclically parthenogenetic Daphnia magna. Male production increased with population density, the major ecological driver of sexual reproduction; however, this response was dampened when the population sex ratio was more male‐biased. Thus, in line with sex ratio theory, we show that D. magna adjust offspring sex allocation in response to the current population sex ratio.     

Males from populations with higher competitive mating success produce sons with lower fitness

Female mate choice can result in direct benefits to the female or indirect benefits through her offspring. Females can increase their fitness by mating with males whose genes encode increased survivorship and reproductive output. Alternatively, male investment in enhanced mating success may come at the cost of reduced investment in offspring fitness. Here, we measure male mating success in a mating arena that allows for male–male, male–female and female–female interactions in Drosophila melanogaster. We then use isofemale line population measurements to correlate male mating success with sperm competitive ability, the number of offspring produced and the indirect benefits of the number of offspring produced by daughters and sons. We find that males from populations that gain more copulations do not increase female fitness through increased offspring production, nor do these males fare better in sperm competition. Instead, we find that these populations have a reduced reproductive output of sons, indicating a potential reproductive trade‐off between male mating success and offspring quality.     

Thelytokous Parthenogenesis in the Fungus-Gardening Ant Mycocepurus smithii (Hymenoptera: Formicidae)

The general prevalence of sexual reproduction over asexual reproduction among organisms testifies to the evolutionary benefits of recombination, such as accelerated adaptation to changing environments and elimination of deleterious mutations. Documented instances of asexual reproduction in groups otherwise dominated by sexual reproduction challenge evolutionary biologists to understand the special circumstances that might confer an advantage to asexual reproductive strategies. Here we report one such instance of asexual reproduction in the ants. We present evidence for obligate thelytoky in the asexual fungus-gardening ant, Mycocepurus smithii, in which queens produce female offspring from unfertilized eggs, workers are sterile, and males appear to be completely absent. Obligate thelytoky is implicated by reproductive physiology of queens, lack of males, absence of mating behavior, and natural history observations. An obligate thelytoky hypothesis is further supported by the absence of evidence indicating sexual reproduction or genetic recombination across the species'' extensive distribution range (Mexico-Argentina). Potential conflicting evidence for sexual reproduction in this species derives from three Mycocepurus males reported in the literature, previously regarded as possible males of M. smithii. However, we show here that these specimens represent males of the congeneric species M. obsoletus, and not males of M. smithii. Mycocepurus smithii is unique among ants and among eusocial Hymenoptera, in that males seem to be completely absent and only queens (and not workers) produce diploid offspring via thelytoky. Because colonies consisting only of females can be propagated consecutively in the laboratory, M. smithii could be an adequate study organism a) to test hypotheses of the population-genetic advantages and disadvantages of asexual reproduction in a social organism and b) inform kin conflict theory.For a Portuguese translation of the abstract, please see Abstract S1.     

Alternative life histories in Xiphophorus multilineatus: evidence for different ages at sexual maturity and growth responses in the wild

In order to examine potential trade-offs in alternative life histories of the high-backed pygmy swordtail Xiphophorus multilineatus, otoliths were used from wild-caught males to determine if sneaker males had the advantage of maturing earlier in natural environments. The sneakers matured significantly earlier than courters, but there was no difference among the three courter variants. In addition, analyses suggested that the effect of the pituitary locus on size at sexual maturity and growth rates was a consequence of age at sexual maturity. Finally, one of the courter variants had a significantly different relationship between age and size at sexual maturity than the other variants, suggesting that in this variant, age at sexual maturity may be more closely related to size and therefore may be less plastic in its growth responses.