An experimental investigation into status-dependent male dimorphism in the European earwig, Forficula auricularia

Discrete alternative reproductive phenotypes are probably often due to individuals adopting alternative tactics with unequal fitnesses in conditional strategies with status-dependent selection. One tactic is believed to be favoured below a status switch point and another tactic above it, owing to different fitness functions of the tactics. Males of the European earwig are dimorphic. Macrolabic males are large (high status) and have long forceps, and brachylabic males are small (low status) with short forceps. I tested whether fitness functions, measured as mating success, of the two morphs differed with regard to forceps length and body weight. Macrolabic males with longer forceps than a competing male had higher mating success but brachylabic males benefited by being heavier than their competitor. Thus, different selection regimes were acting on the two morphs, suggesting that their fitness functions differed in relation to status. These observations and those of previous studies, showing that morph expression is environmentally determined and is associated with body size and that the morphs have unequal fitness, provide support for the hypothesis that male dimorphism in this species is a conditional strategy that has evolved under status-dependent selection. The differential investment in forceps growth that characterizes the morphs was manifested in a steeper allometric relation between forceps length and body size in macrolabic than brachylabic males. Behavioural observations showed that males of both morphs engaged in direct contests for females. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Structural complexity of the environment affects the survival of alternative male reproductive tactics

Alternative reproductive tactics in males are often associated with divergent phenotypes expressed as phenotypically plastic threshold traits. The evolution of threshold traits in these species has been modeled under the conditional evolutionarily stable strategy (ESS). Both strategic and genetic models predict that perturbations to the fitness trade-off between the male morphs will lead to a shift in the ESS switch point of the threshold. So far, demographic factors that influence the competitive ability of male morphs have been investigated and related to intraspecific population variation in male dimorphic thresholds. Here we reveal evidence for the theoretical prediction that abiotic features of the environment, in particular its structural complexity, are likely to influence the ESS threshold. In the male dimorphic mite Sancassania berlesei, we monitored the survival of aggressive fighter males and their benign scrambler counterparts in populations that differed in structural complexity. We found that, consistent with our prediction, the complex habitat favored fighter males, enabling them to kill a greater number of rival scramblers. We found no effect of habitat complexity on the survival of fighter males. These results demonstrate how abiotic as well as biotic aspects of the environment can be important in determining the frequencies of males adopting alternative tactics in different species or populations.     

Conditional male dimorphism and alternative reproductive tactics in a Neotropical arachnid (Opiliones)

In arthropods, most cases of morphological dimorphism within males are the result of a conditional evolutionarily stable strategy (ESS) with status-dependent tactics. In conditionally male-dimorphic species, the status’ distributions of male morphs often overlap, and the environmentally cued threshold model (ET) states that the degree of overlap depends on the genetic variation in the distribution of the switchpoints that determine which morph is expressed in each value of status. Here we describe male dimorphism and alternative mating behaviors in the harvestman Serracutisoma proximum. Majors express elongated second legs and use them in territorial fights; minors possess short second legs and do not fight, but rather sneak into majors’ territories and copulate with egg-guarding females. The static allometry of second legs reveals that major phenotype expression depends on body size (status), and that the switchpoint underlying the dimorphism presents a large amount of genetic variation in the population, which probably results from weak selective pressure on this trait. With a mark-recapture study, we show that major phenotype expression does not result in survival costs, which is consistent with our hypothesis that there is weak selection on the switchpoint. Finally, we demonstrate that switchpoint is independent of status distribution. In conclusion, our data support the ET model prediction that the genetic correlation between status and switchpoint is low, allowing the status distribution to evolve or to fluctuate seasonally, without any effect on the position of the mean switchpoint.     

Ownership-dependent mating tactics of minor males of the beetle <Emphasis Type="Italic">Librodor japonicus</Emphasis> (Nitidulidae) with intra-sexual dimorphism of mandibles

Intra-sexual dimorphism is found in the weapons of many male beetles. Different behavioral tactics to access females between major and minor males, which adopt fighting and alternative tactics, respectively, are thought to maintain the male dimorphism. In these species major males have enlarged weapons that they use in fights with rival males. Minor males also have small weapons in some of these species, and it is unclear why these males possess weapons. We examined the hypothesis that minor males might adopt a fighting tactic when their status was relatively high in comparison with that of other males (e.g., ownership of a territory). We observed the behavioral tactics of major and minor males of the beetle Librodor japonicus, whose males have a dimorphism of their mandibles. Major males fought for resources, whereas minor males adopted two status-dependent tactics, fighting and sneaking, to access females, depending on their ownership of a sap site. We suggest that ownership status-dependent mating tactics in minor males may maintain the intra-sexual dimorphism in this beetle.     

Male sand crickets trade-off flight capability for reproductive potential

In this paper, we test the hypothesis that male sand crickets, Gryllus firmus, experience a trade-off between flight capability and reproductive potential expressed as reduced testis weight in flight-capable morphs. We used a half-sib design with 130 sires, three dams per sire and an average of 5.66 males per dam family, for a total of 2206 F1 offspring. Traits measured were head width, somatic dry weight, testis weight, wing morph (micropterous/macropterous), weight of the dorso-longitudinal flight muscles (DLM) and the functional status of these muscles. Heritabilities of all traits were significant and ranged from 0.14 to 0.43. All traits were positively correlated with body size, but removal of this covariance revealed a highly significant trade-off, both phenotypically and genetically, between testes size and flight capability as measured by wing morph, DLM size or DLM status. The possible implications of this for morph-specific reproductive tactics are discussed.     

Males influence maternal effects that promote sexual selection: a quantitative genetic experiment with dung beetles Onthophagus taurus

Recently, doubt has been cast on studies supporting good genes sexual selection by the suggestion that observed genetic benefits for offspring may be confounded by differential maternal allocation. In traditional analyses, observed genetic sire effects on offspring phenotype may result from females allocating more resources to the offspring of attractive males. However, maternal effects such as differential allocation may represent a mechanism promoting genetic sire effects, rather than an alternative to them. Here we report results from an experiment on the horned dung beetle Onthophagus taurus, in which we directly compare genetic sire effects with maternal effects that are dependent on sire phenotype. We found strong evidence that mothers provide more resources to offspring when mated with large-horned males. There were significant heritabilities for both horn length and body size, but when differential maternal effects were controlled, the observed estimates of genetic variance were greatly reduced. Our experiment provides evidence that differential maternal effects may amplify genetic effects on offspring traits that are closely related to fitness. Thus, our results may partly explain the relatively high coefficients of additive genetic variation observed in fitness-related traits and provide empirical support for the theoretical argument that maternal effects can play an important role in evolution.     

Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra‐pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within‐pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra‐pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade‐off between male within‐pair paternity success and extra‐pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.     

Life-history consequences of bidirectional selection for male morph in a male-dimorphic bulb mite

Intralocus sexual conflict (IASC) arises when males and females have different trait optima. Some males pursue different alternative reproductive tactics (ARTs) with different trait optima, resulting in different strengths of IASC. Consequently, for instance daughter fitness is differentially affected by her sire’s morph. We tested if—and which—other life-history traits correlatively change in bidirectional, artificial selection experiments for ARTs. We used the male-dimorphic bulb mite Rhizoglyphus robini, the males of which are high-fitness ‘fighters’ or low-fitness ‘scramblers’. Twice in each of the five generations of selection, we assessed clutch composition (number of mites of the various life stages present) and size (total number of offspring). Furthermore, we tracked offspring from egg to adulthood in the first and final generation to detect differences between selection lines in the size and duration of stages, and in maturation time. We found that selection for male morph increased the frequency of that morph. Furthermore, compared to fighter lines, scrambler lines produced more females, which laid larger eggs (in the final generations), and maintained a higher egg-laying rate for longer. Otherwise, our results showed no consistent differences between the selection lines in clutch size and composition, life stage size or duration, or maturation time. Though we found few correlated life-history trait changes in response to selection on male morph, the differences in egg laying rate and egg size suggest that IASC between fighters is costlier to females than IASC with scramblers. We hypothesize that these differences in reproductive traits allow fighter-offspring to perform better in small, declining populations but scrambler-offspring to perform better in large, growing populations.     

The mechanisms of morph determination in the amphipod Jassa: implications for the evolution of alternative male phenotypes

The proximal basis for and the maintenance of alternative male reproductive strategies and tactics are generally not understood in most species, despite the occurrence of male polymorphism across many taxa. In the marine amphipod Jassa marmorata, males differ in morphology as well as behaviour. This dimorphism corresponds to two contrasting reproductive strategies: small sneaker males or 'minors', and large fighter males or 'majors'. This study uses quantitative genetic analyses in conjunction with experimental manipulations to assess the relative importance of genetic versus environmental factors in the determination and maintenance of these alternative mating strategies. Heritability analyses indicated the reproductive phenotypes do not reflect genetic differences between dimorphic males. By contrast, morph determination was significantly affected by diet quality. Majors essentially only developed on high-protein diets. Field studies also identified a strong correlation between seasonal shifts in the relative proportions of morphs and changes in food (i.e. phytoplankton) quantity and composition, corroborating that diet cues the switch between alternative reproductive tactics. Moreover, the comparison of major and minor growth trajectories identified a heterochronic shift in maturation times between morphs, indicating that ecological selective pressures, rather than just sexual selection, may be involved in the maintenance of this conditional strategy.     

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

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

Status-dependent selection in the dimorphic beetle Onthophagus taurus.

The occurrence of alternative reproductive phenotypes is widespread in most animal taxa. The majority of known examples best fit the notion of alternative tactics within a conditional strategy where the fitness pay-offs depend on an individual's competitive ability or status. Individuals are proposed as "choosing" the tactic that maximizes their fitness, given their status relative to others in the population. Theoretically, status-dependent selection should determine when an animal should switch between alternative tactics. While a number of studies have demonstrated unequal fitness pay-offs associated with alternative tactics, none, to our knowledge, have examined the fitness functions necessary for predicting when individuals should switch between tactics. Here, we use a dimorphic male beetle in order to provide the first empirically derived fitness function across alternative reproductive phenotypes. Our data provide empirical support for a game-theoretic conditional strategy that has evolved under status-dependent selection.     

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.     

THE EFFECTS OF THE MATING SYSTEM ON PROGENY PERFORMANCE IN HYLA CRUCIFER (ANURA: HYLIDAE)

We performed a controlled mating experiment to determine whether genetic variation in larval traits in Hyla crucifer was predictable on the basis of mating status or body size of male parent. Larval growth rate was predictably related to body size of the sire. Males from the upper half of the body-size distribution sired offspring with 6% higher growth rates than those of offspring sired by males from the lower half of the body-size distribution. Offspring sired by males that obtained mates in nature had 3% higher growth rates than their half-siblings sired by males that did not mate in nature. Genetic variation for larval-period duration and size at metamorphosis was detected; however, neither mating status nor body size of sire could be used to predict values of these traits in the progeny. Although all three larval traits can affect fitness, there was no evidence that the offspring of some sires would always outperform the offspring of others in all three traits. The predictable association between adult male size and larval growth rate means that the H. crucifer mating system would have a directional effect on larval growth rate if male body size influences the outcome of male-male competition or female choice.     

Alternative reproductive tactics are associated with sperm performance in invasive round goby from two different salinity environments

During male–male competition, evolution can favor alternative reproductive tactics. This often results in a dominant morph that holds a resource, such as a nest for egg laying, which competes with a smaller sneaker morph that reproduces by stealing fertilizations. The salinity environment can influence male growth rates, for example, via osmoregulatory costs, which in turn may influence the use of sneaker tactics for small males competing for mating opportunities. Salinity can also affect sperm directly; however, little is known of how salinity influences sneaker tactics through sperm performance. We sampled males of the invasive round goby (Neogobius melanostomus) from two environments, a freshwater river and a brackish estuary. This fish has two male morphs: nest‐holding dark males and non‐nest‐holding light males. We examined the role of water salinity of 0, 8, and 16 on sperm performance and found that for estuarine males, a salinity of 0 reduced sperm velocity compared to a salinity of 8 and 16. Riverine males had low velocity in all salinities. Sperm viability also decreased by over 30% in 0 salinity, compared to 8 and 16, for fish from both environments. Gobies produce ejaculate contents in specialized glands that could in theory shield sperm in an adverse environment. However, gland contents did not improve sperm performance in our tests. Body mass and age estimates indicate that riverine males invested more in somatic growth compared to estuarine males. Estuarine light morph males had a high enough gonadosomatic index to indicate sneaker tactics. We propose that when sperm performance is low, such as for the riverine males, sneaker tactics are ineffective and will be selected against or phenotypically suppressed. Instead, we interpret the increased investment in somatic growth found in riverine males as a life‐history decision that is advantageous when defending a nest in the next reproductive season.     

Molecular insight into patterns of colony composition and paternity in the common mole-rat Cryptomys hottentotus hottentotus

We report the discovery of intraspecific variation in both colony composition and patterns of paternity in two populations of the social common mole-rat Cryptomys hottentotus hottentotus. These two populations represent the mesic and arid habitat extremes of the species' broad ecological range in South Africa. Until recently colonies of the common mole-rat were thought to consist of familial groups whereby all colony members were the offspring of a monogamous reproductive pair. The remaining colony members were thought to forego reproduction until both social and ecological conditions favoured dispersal and opportunities for independent outbreeding. Results from genetic assignment tests using microsatellite markers indicate that while colony composition is dominated by familial groups, colonies within both populations included both adult and subadult foreign conspecifics. Analysis of parentage reveals that the social organization of C. h. hottentotus is not that of strict monogamy; paternity of offspring was not assigned consistently to the largest, most dominant male within the colony. Moreover, a number of significantly smaller males were found to sire offspring, suggesting a sneak-mating strategy by subordinate within-colony males. Extra-colony extra-pair paternity (ECP) was also found to characterize C. h. hottentotus colonies, occurring with similar frequencies in both habitats. Both dominant established breeding males and subordinate males were identified as siring young in nonsource colonies. Furthermore, established breeding males were found to sire extra-colony young in the same season as siring young within their source colonies. We discuss the significance of these results within the context of the divergent ecological regimes characterizing the two sites and observe that our results revisit the accuracy of using behavioural and morphological characters, which have structured the basis of our understanding of the behavioural ecology of this species, as indicators of breeding status in mark-recapture studies.     

SEXUAL SELECTION IN AMERICAN TOADS: A TEST OF A GOOD-GENES HYPOTHESIS

Adaptive mate choice in species lacking male resource control and/or paternal care might be maintained by selection because preferred males sire genetically superior offspring. For such a process to occur, some male phenotypic trait(s) must both reliably indicate male genetic quality and influence the pattern of mate choice by females. In American toads, Bufo americanus, male body length has been documented to influence female mating patterns: females usually mate with males that are larger than average. However, the relationship between male size and male genetic quality is unknown. We conducted a controlled breeding experiment using 48 sires and 19 dams to determine if larger males sire offspring with superior larval performance characteristics (greater survival to metamorphosis, larger mass at metamorphosis, and earlier metamorphosis). We also aged each sire to test the hypothesis that older males are, on average, genetically superior to younger males. We crossed each female with three sires representing three body size categories (mean and 1 SD ± mean snout-ischium length). Hatchlings (500 from each cross) were reared to metamorphosis in seminatural ponds in the field. Metamorph weight (log transformed) and age at metamorphosis showed significant heritability and were genetically correlated with each other. Hence, sires differed in genetic quality. However, none of the three measures of offspring performance was correlated with sire body size or age. Thus, we obtained no support for the prediction that sire body size or age is related to genetic quality.     

Status‐dependence and morphological trade‐offs in the expression of a sexually selected character in the mite,Sancassania berlesei

Abstract In the male dimorphic mite Sancassania berlesei, fighter males kill rivals with a pair of armoured legs whereas scrambler males are benign with unmodified legs. In an adaptive response mediated by colony pheromones, fighter expression increases at low colony density. Under the status‐dependent evolutionarily stable strategy (ESS) model we expected heavier final instar nymphs to become fighters. This was supported in group reared nymphs. In individually reared nymphs fighter expression was experimentally suppressed using two concentrations of colony pheromone. Here, male morph expression again depended on tritonymphal body mass and contact is therefore unnecessary for individuals to judge their status. Fighter suppression was greater in the higher pheromone treatment, but morph determination remained status dependent. The weight and length of fighters was lower than scramblers of same‐weight final instar nymphs, indicating a developmental trade‐off, and a cost not recouped at the adult stage.     

Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly

Although colour polymorphisms in adult organisms of many taxa are often adaptive in the context of sexual selection or predation, genetic correlations between colour and other phenotypic traits expressed early in ontogeny could also play an important role in polymorphic systems. We studied phenotypic and genetic variation in development time among female colour morphs in the polymorphic damselfly Ischnura elegans in the field and by raising larvae in a common laboratory environment. In the field, the three different female morphs emerged at different times. Among laboratory-raised families, we found evidence of a significant correlation between maternal morph and larval development time in both sexes. This suggests that the phenotypic correlation between morph and emergence time in the field has a parallel in a genetic correlation between maternal colour and offspring development time. Maternal colour morph frequencies could thus potentially change as correlated responses to selection on larval emergence dates. The similar genetic correlation in male offspring suggests that sex-limitation in this system is incomplete, which may lead to an ontogenetic sexual conflict between selection for early male emergence (protandry) and emergence times associated with maternal morph.     

The evolution of parental care in the context of sexual selection: a critical reassessment of parental investment theory

Males and females are often defined by differences in their energetic investment in gametes. In most sexual species, females produce few large ova, whereas males produce many tiny sperm. This difference in initial parental investment is presumed to exert a fundamental influence on sex differences in mating and parental behavior, resulting in a taxonomic bias toward parental care in females and away from parental care in males. In this article, we reexamine the logic of this argument as well as the evolutionarily stable strategy (ESS) theory often used to substantiate it. We show that the classic ESS model, which contrasts parental care with offspring desertion, violates the necessary relationship between mean male and female fitness. When the constraint of equal male and female mean fitness is correctly incorporated into the ESS model, its results are congruent with those of evolutionary genetic theory for the evolution of genes with direct and indirect effects. Male parental care evolves whenever half the magnitude of the indirect effect of paternal care on offspring viability exceeds the direct effect of additional mating success gained by desertion. When the converse is true, desertion invades and spreads. In the absence of a genetic correlation between the sexes, the evolution of paternal care is independent of maternal care. Theories based on sex differences in gametic investment make no such specific predictions. We discuss whether inferences about the evolution of sex differences in parental care can hold if the ESS theory on which they are based contains internal contradictions.     

Male Investments in High Quality Sperm Improve Fertilization Success,but May Have Negative Impact on Offspring Fitness in Whitefish

Many ejaculate traits show remarkable variation in relation to male social status. Males in disfavoured (subordinate) mating positions often invest heavily on sperm motility but may have less available resources on traits (e.g., secondary sexual ornaments) that improve the probability of gaining matings. Although higher investments in sperm motility can increase the relative fertilization success of subordinate males, it is unclear whether status-dependent differences in sperm traits could have any consequences for offspring fitness. We tested this possibility in whitefish (Coregonus lavaretus L.) by experimentally fertilizing the eggs of 24 females with the sperm of either highly-ornamented (large breeding tubercles, dominant) or less-ornamented (small tubercles, subordinate) males (split-clutch breeding design). In comparison to highly-ornamented individuals, less-ornamented males had higher sperm motility, which fertilized the eggs more efficiently, but produced embryos with impaired hatching success. Also offspring size and body condition were lower among less-ornamented males. Furthermore, sperm motility was positively associated with the fertilization success and offspring size, but only in highly-ornamented males. Together our results indicate that male investments on highly motile (fertile) sperm is not necessarily advantageous during later offspring ontogeny and that male status-dependent differences in sperm phenotype may have important effects on offspring fitness in different life-history stages.