Sex differences in the effects of juvenile and adult diet on age‐dependent reproductive effort

Sexual selection should cause sex differences in patterns of resource allocation. When current and future reproductive effort trade off, variation in resource acquisition might further cause sex differences in age‐dependent investment, or in sensitivity to changes in resource availability over time. However, the nature and prevalence of sex differences in age‐dependent investment remain unclear. We manipulated resource acquisition at juvenile and adult stages in decorated crickets, Gryllodes sigillatus, and assessed effects on sex‐specific allocation to age‐dependent reproductive effort (calling in males, fecundity in females) and longevity. We predicted that the resource and time demands of egg production would result in relatively consistent female strategies across treatments, whereas male investment should depend sharply on diet. Contrary to expectations, female age‐dependent reproductive effort diverged substantially across treatments, with resource‐limited females showing much lower and later investment in reproduction; the highest fecundity was associated with intermediate lifespans. In contrast, long‐lived males always signalled more than short‐lived males, and male age‐dependent reproductive effort did not depend on diet. We found consistently positive covariance between male reproductive effort and lifespan, whereas diet altered this covariance in females, revealing sex differences in the benefits of allocation to longevity. Our results support sex‐specific selection on allocation patterns, but also suggest a simpler alternative: males may use social feedback to make allocation decisions and preferentially store resources as energetic reserves in its absence. Increased calling effort with age therefore could be caused by gradual resource accumulation, heightened mortality risk over time, and a lack of feedback from available mates.     

Dangerous love? Predation risk does not affect female mate choice in blue‐black grassquits

Predation risk may be an important factor affecting female mate choice. Hypothetically, females could choose extravagantly ornamented males that survive in high predation risk environments. However, this decision could be different if choosing a conspicuous male under high predation risk is costly for females or results in reduced offspring survival. In such contexts, females could become indifferent to male quality or prefer inconspicuous males. We tested this idea using captive blue‐black grassquits (Volatinia jacarina, Linnaeus, 1766), a species in which males perform conspicuous leap displays coupled with songs during the breeding season, which presumably subjects females and offspring to higher predation risk. Females were placed in an arena with speakers on opposite sides emitting male courtship songs. One speaker emitted songs at a high rate (proxy for a conspicuous male) while the other speaker broadcast songs at a low rate (proxy for a less conspicuous male). While the female evaluated the two male songs, a third speaker emitted vocalizations characterizing three levels of risk: adult predator, nest predator, and no‐risk control. Females showed no preference for either male stimuli across the predation risk treatments. This lack of preference relative to frequency of male vocal displays suggests that leap‐song frequency is not used by females during mate choice. We suggest that in addition to its role in courtship, male grassquit displays also signal status to other males when competing for territories. Thus, we propose that predation risk does not directly influence blue‐black grassquit intersexual selection and that females in this species may exercise indirect mate choice, choosing social mates based on male ability to establish and defend a territory, and relying secondarily upon other aspects of male display attributes, such as its visual components.     

Plasticity of the phonotactic selectiveness of four species of chirping crickets (Gryllidae): Implications for call recognition

Earlier studies of phonotaxis by female crickets describe this selective behavioural response as being important in the females' choices of conspecific males, leading to reproduction. In the present study, moderate (30+) to very large data sets of phonotactic behaviour by female Acheta domesticus L., Gryllus bimaculatus DeGeer, Gryllus pennsylvanicus Burmeister and Gryllus veletis Alexander demonstrate substantially greater plasticity in the behavioural choices, as made by females of each species, for the syllable periods (SP) of model calling songs (CS) than has been previously described. Phonotactic choices by each species range from the very selective (i.e. responding to only one or two SPs) to very unselective (i.e. responding to all SPs presented). Some females that do not respond to all SPs prefer a range that includes either the longest or shortest SP tested, which fall outside the range of SPs produced by conspecific males. Old female A. domesticus and G. pennsylvanicus are more likely to be unselective for SPs than are young females. Each species includes females that do not respond to a particular SP when responding to CSs with longer and shorter SPs. The results suggest that the plasticity of phonotactic behaviour collectively exhibited by the females of each species does not ensure that choices of a male's CS effectively focus the female's phonotactic responses on CSs that represent the conspecific male. The phonotactic behaviour collectively exhibited by females of each species does not readily fit any of the models for selective processing by central auditory neurones that have been proposed to underlie phonotactic choice.     

Temporal Shifts in Conspicuousness: Mate Attraction Displays of the Texas Field Cricket, Gryllus texensis

Conspicuous mate attraction displays can simultaneously draw the attention of potential mates and predators, placing the signaller in peril of becoming prey. The balance between these countervailing forms of selection has the potential to shape mate attraction displays. Male Texas field crickets (Gryllus texensis; Orthoptera) signal acoustically to attract mates. Mating signals also attract acoustically orienting parasitoid flies (Ormia ochracea; Tachinidae). Both the abundance of female crickets and parasitoid flies fluctuates throughout the night. We show mate attraction displays exhibit diel shifts that correlate positively with expected female cricket presence and negatively with expected parasitoid fly activity. During early evening, when parasitoids are most common and mating is scarce, crickets signal less often and with reduced conspicuousness. During the second half of the evening, when sexually receptive females are abundant and parasitoids are scarce, crickets signal more often and with enhanced conspicuousness. These diel shifts in mate attraction displays do not appear to result from male crickets detecting parasitoid flies or female crickets and altering their behaviour accordingly. Males in close proximity to parasitoid flies or female crickets do not signal differently than lone males. Instead, diel pattern shifts in mate attraction displays appear to be a selective response to trade‐offs between natural selection via parasitism and sexual selection via mate choice.     

The influence of female age on phonotaxis during single and multiple song presentations in the field cricket,Gryllus integer (Orthoptera: Gryllidae)

The influence of age on variation in female phonontaxis in the field cricket,Gryllus integer, was investigated using a Kugel treadmill-type device. Synthetic male calling songs, with different pulse rates, were presented in both single-stimulus and three-stimulus designs. Females were either 11–14 or 25–28 days postecdysis. Females varied in motivation, or the degree of reproductive effort they exhibited, but only in single-stimulus trials: older females achieved higher scores than younger females. Females varied in selectivity, or the extent to which they discriminated among potential mates, in both presentation designs. All females discriminated against atypical pulse rates. In multiple-stimulus trials with normal range pulse rates, younger females were discriminatory; older females were not. Mated females showed reduced phonotaxis and selectivity irrespective of mating interval.     

INBREEDING AND ADVERTISEMENT CALLING IN THE CRICKET TELEOGRYLLUS COMMODUS: LABORATORY AND FIELD EXPERIMENTS

If sexually selected traits reveal a male's heterozygosity or condition to females, then such traits should exhibit declines with inbreeding. We tested this by examining the effect of inbreeding on advertisement calling in male crickets Teleogryllus commodus. We investigated the effect of one generation of full‐sibling mating on calling effort and fine‐scale call structure. Inbreeding reduced calling effort but had no effect on call structure. We then compared the attractiveness of inbred and outbred calls in the field by monitoring how many wild females were attracted to each call type. From the field data, we conducted a selection analysis to identify the major axes of linear and nonlinear multivariate sexual selection on call structure. A comparison of multivariate attractiveness of inbred and outbred calls along each major axis of selection revealed no difference in attractiveness. Our results suggest that inbred male calls have a fine‐scale structure that is no less attractive to females than that of outbred calls. However, because inbred males call less often, and female T. commodus prefer males with a higher calling effort, inbred males will suffer reductions in mating success. Females who base mate choice on call rate are therefore using a signal correlated with male heterozygosity and/or condition.     

The influence of auditory and visual experience on the phonotactic behavior of the cricket,Gryllus bimaculatus

Female crickets lacking experience with phonotaxis to conspecific calling song respond to trains of continuously repeated sound pulses (trill), whereas experienced females do not. In the present study such inexperienced crickets were tested for their responsiveness to trills of pulse repetition periods from 30 to 70 ms on a Y- shaped maze. Stimulation with a repetition period of 30 ms led to unexpectedly low phonotactic and exploratory activity. Initial stimulation with trills of 30- ms repetition period drastically reduced the responsiveness of inexperienced animals to conspecific calling song and other attractive stimuli. Effects of visual stimulation on the phonotactic behavior of female crickets are demonstrated. Threatening visual stimuli changed the behavior of experienced animals to a state that resembles that of inexperienced animals. The relevance of these observations is discussed with respect to the development of the auditory pattern recognition mechanism in crickets.     

Long‐distance signals influence assessment of close range mating displays in the field cricket,Gryllus integer

Male sexual displays often include components detected across long distances, and those perceived only at close range. Understanding what information females gain from each component of a complex display and how they use these signals to make decisions are questions of major interest in sexual selection research. We evaluated content‐based hypotheses (‘redundant signals’ and ‘multiple messages’) for the courtship displays of field crickets (Gryllus integer) by measuring female responses to males' long‐distance calling song (calls) and close‐range chemical cues. Females' responses to a male's calls and chemical cues were uncorrelated, supporting the ‘multiple messages’ hypothesis. We also tested the ‘inter‐signal interaction’ hypothesis by investigating how long‐distance calls influence evaluation of close‐range courtship. The relationship between long‐ and close‐range signals was complex and conditional: females accepted close‐range courtship more quickly after exposure to attractive calling song than they did after exposure to either unattractive calling song or silence, and unattractive calls were no more or less effective than silence. This inter‐signal interaction could affect our understanding of mate choice in species with multiple mating signals because it implies that females may save time and energy by not assessing the close‐range signals of attractive long‐distance signalers. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 856–865.     

Female choice for male cuticular hydrocarbon profile in decorated crickets is not based on similarity to their own profile

Indirect genetic benefits derived from female mate choice comprise additive (good genes) and nonadditive genetic benefits (genetic compatibility). Although good genes can be revealed by condition‐dependent display traits, the mechanism by which compatibility alleles are detected is unclear because evaluation of the genetic similarity of a prospective mate requires the female to assess the genotype of the male and compare it to her own. Cuticular hydrocarbons (CHCs), lipids coating the exoskeleton of most insects, influence female mate choice in a number of species and offer a way for females to assess genetic similarity of prospective mates. Here, we determine whether female mate choice in decorated crickets is based on male CHCs and whether it is influenced by females' own CHC profiles. We used multivariate selection analysis to estimate the strength and form of selection acting on male CHCs through female mate choice, and employed different measures of multivariate dissimilarity to determine whether a female's preference for male CHCs is based on similarity to her own CHC profile. Female mating preferences were significantly influenced by CHC profiles of males. Male CHC attractiveness was not, however, contingent on the CHC profile of the choosing female, as certain male CHC phenotypes were equally attractive to most females, evidenced by significant linear and stabilizing selection gradients. These results suggest that additive genetic benefits, rather than nonadditive genetic benefits, accrue to female mate choice, in support of earlier work showing that CHC expression of males, but not females, is condition dependent.     

Can MHC‐assortative partner choice promote offspring diversity? A new combination of MHC‐dependent behaviours among sexes in a highly successful invasive mammal

Sexual selection involving genetically disassortative mate choice is one of several evolutionary processes that can maintain or enhance population genetic variability. Examples of reproductive systems in which choosers (generally females) select mates depending on their major histocompatibility complex (MHC) genes have been reported for several vertebrate species. Notably, the role of MHC‐dependent choice not in mating contexts, but in other kinds of social interactions such as in the establishment of complex social systems, has not yet drawn significant scientific interest and is virtually absent from the literature. We have investigated male and female MHC‐dependent choice in an invasive population of North American raccoons (Procyon lotor) in Germany. Both male and female raccoons rely on olfaction for individual recognition. Males have an unusually complex social system in which older individuals choose unrelated younger ones to form stable male coalitions that defend territories and a monopoly over females. We have confirmed that females perform MHC‐disassortative mate choice and that this behaviour fosters genetic diversity of offspring. We have also observed that males build coalitions by choosing male partners depending on their MHC, but in an assortative manner. This is the first observation of antagonistic MHC‐dependent behaviours among sexes. We show that this is the only combination of MHC‐dependent partner choice that leads to outbreeding. In the case of introduced raccoons, such behaviours can act together to promote the invasive potential of the species by increasing its adaptive genetic divergence.     

Mate Quality and Novelty Influence Post‐Copulatory Female Choice in Decorated Crickets,Gryllodes sigillatus

Females of many taxa prefer to mate with novel males rather than previous mates, but also favor males that have traits indicative of higher genetic quality or compatibility. However, it may not be possible for females to simultaneously choose males that are both novel and of high quality, and the female response to this dilemma has not previously been examined. In this paper, we ask whether female decorated crickets, Gryllodes sigillatus, exert their choice for novel males via post‐copulatory choice (sperm ampulla removal) and whether male genetic background (variation in male quality) affects this decision. We found that after matings with inbred males, females removed the ampullae of familiar mates sooner than those of novel males, whereas after matings with outbred males, there was no difference in the ampulla‐retention times of familiar mates and novel partners. This suggests that when male do not vary in quality, females prefer novel partners. However, when males vary in quality, female preferences for male traits are more important than preferences for novel partners.     

Secondary compounds from exotic tree plantations change female mating preferences in the palmate newt (Lissotriton helveticus)

Selection can favour phenotypic plasticity in mate choice in response to environmental factors that alter the costs and benefits of being choosy, or of choosing specific mates. Human‐induced environmental change could alter sexual selection by affecting the costs of mate choice, or by impairing the ability of individuals to identify preferred mates. For example, variation in mate choice could be driven by environmentally induced differences in body condition (e.g. health) that change the cost of choosiness, or by environmental effects on the ability to detect or discriminate sexual signals. We teased apart these possibilities experimentally, by comparing female mate choice in the palmate newt Lissotriton helveticus between environments that mimic water from either native oak forests or exotic eucalypt plantations. In laboratory two‐choice mate trials in clean water, females with prolonged exposure (21 days) to waterborne chemicals leached from eucalypt leaves did not preferentially associate with the male with a stronger immune response, but females exposed to water with chemicals from oak leaves did. In contrast, female choice was unaffected by the immediate presence or absence of eucalypt leachates during mate choice (using only females previously held in oak‐treated water). The habitat‐related change in female choice we observed is likely to be driven by effects of eucalypt leachates on female physiology, rather than immediate inhibition of pheromone transmission or blocking of pheromone reception.     

Replicated evolutionary divergence in the cuticular hydrocarbon profile of male crickets associated with the loss of song in the Hawaiian archipelago

Female choice based on male secondary sexual traits is well documented, although the extent to which this selection can drive an evolutionary divergence in male traits among populations is less clear. Male field crickets Teleogryllus oceanicus attract females using a calling song and once contacted switch to courtship song to persuade them to mate. These crickets also secrete onto their cuticle a cocktail of long‐chained fatty acids or cuticular hydrocarbons (CHCs). Females choose among potential mates based on the structure of male acoustic signals and on the composition of male CHC profiles. Here, we utilize two naturally occurring mutations that have arisen independently on two Hawaiian islands and render the male silent to ask whether the evolutionary loss of acoustic signalling can drive an evolutionary divergence in the alternative signalling modality, male CHC profiles. Q_ST‐F_ST comparisons revealed strong patterns of CHC divergence among three populations of crickets on the islands of Hawaii, Oahu and Kauai. Contrasts between wild‐type and flatwing males on the islands of Oahu and Kauai indicated that variation in male CHC profiles within populations is associated with the loss of acoustic signalling; flatwing males had a relatively low abundance of long‐chained CHCs relative to the short‐chained CHCs that females find attractive. Given their dual functions in desiccation resistance and sexual signalling, insect CHCs may be particularly important traits for reproductive isolation and ultimately speciation.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

The Effect of Age on a Sexually Selected Acoustic Display

Models of sexual selection suggest that females should prefer to mate with older males because old age is evidence of heritable high viability. In a longitudinal analysis, we demonstrate that male field crickets (Gryllus campestris) alter their calling song with age. Carrier frequency, a calling song character related to growing condition and the main song component under female preference, changed towards higher sexual attractiveness with age. Body mass decreased slightly with age, while chirp rate, an indicator of current condition, remained stable. By choosing males singing at a low frequency, female field crickets would base their mate choice decision on a sexual trait that indicates superior growing conditions as juvenile and on viability, i.e. enhanced current condition as adult.     

No Coolidge Effect in Decorated Crickets

Female decorated crickets, Gryllodes sigillatus , obtain genetic benefits by mating with different males and, when given a choice, prefer novel males over previous mates. It is unknown, however, whether males exhibit a similar preference for novel females. Although female crickets control copulation, there are at least two ways in which males can exercise choice: (1) the amount of courtship directed towards prospective mates and (2) the size of the spermatophore transferred to the female at mating. To determine whether males devote more courtship effort to novel females while controlling for female behavioral cues, male courtship effort toward two dead females, one, a previous mate and the other, a novel female, was measured. To determine whether males manufacture larger spermatophores when paired with novel females, males were mated to novel or previous mates, and the different components of the spermatophore weighed. Males did not spend more time courting dead novel females than previous mates. There was no difference in the latency to remating of males confined with novel females and those paired with previous mates, and there was no difference in the mass of spermatophores transferred to novel and familiar females. Contrary to previous studies in other taxa, this study suggests that male crickets do not prefer novel mates and thus, are not subject to the Coolidge effect. Although mating with novel females may be beneficial to males, selection on males to identify and discriminate against previous mates may be relaxed because of a strong female preference for novel males.     

The importance of calling song and courtship song in female mate choice in the variable field cricket

Male field crickets produce calling songs, courtship songs, tactile signals and chemical signals. Although calling songs are known to play an important role in female mate choice, the importance of the other signals in mate choice is poorly understood. In the variable field cricket, Gryllus lineaticeps, females select mates, in part, based on variation in male calling song. Females prefer higher chirp rates, a trait which is partially dependent on male nutrient intake, and females prefer longer chirp durations, a trait which appears to be independent of male nutrient intake. We tested whether females also have preferences based on variation in male courtship song, and whether the structure of male courtship song varies with nutrient intake. First, we reexamined female preference for calling song chirp rate. Then, we examined: (1) female preference based on courtship song chirp rate; (2) the relative importance of calling song and courtship song chirp rate; (3) the nutrition dependence of courtship song chirp rate; and (4) the correlation between calling song and courtship song chirp rate. As reported previously, females preferred higher calling song chirp rates, and in addition, preferred higher courtship song chirp rates. Females were more likely to switch from a speaker broadcasting more attractive calling song to a speaker broadcasting less attractive calling song when the attractive calling song was associated with an unattractive courtship song than when it was associated with an attractive courtship song. Preferences based on courtship song may thus cause females to alter the choices that they made based on calling song. Males that received greater nutrients did not produce higher courtship song chirp rates. There was no correlation between calling song and courtship song chirp rate. As a result, the two traits may provide information to females about different aspects of male quality. Copyright 2000 The Association for the Study of Animal Behaviour.     

Beyond temperature coupling: Effects of temperature on ectotherm signaling and mate choice and the implications for communication in multispecies assemblages

Many organisms share communication channels, generating complex signaling environments that increase the risk of signal interference. Variation in abiotic conditions, such as temperature, may further exacerbate signal interference, particularly in ectotherms. We tested the effects of temperature on the pulse rate of male signals in a community of Oecanthus tree crickets, and for one focal species we also assessed its effect on female pulse rate preferences and motivation to seek mates. We confirm prior findings of temperature‐dependent signals that result in increasing signal similarity at lower temperatures. Temperature also affected several aspects of female preferences: The preferred pulse rate value was temperature dependent, and nearly perfectly coupled with signal pulse rate; the range of pulse rate values that females found attractive also increased with temperature. By contrast, the motivation of females to perform phonotaxis was unaffected by temperature. Thus, at lower temperatures the signals of closely related species were more similar and females more discriminating. However, because signal similarity increased more strongly than female discrimination, signal interference and the likelihood of mismating may increase as temperatures drop. We suggest that a community approach will be useful for understanding the role of environmental variability in the evolution of communication systems.     

Modulation of syllable period‐selective phonotaxis by prothoracic neurones in crickets (Acheta domesticus): juvenile hormone,picrotoxin and photoinactivation of the ON1 neurones

Abstract In response to model calling songs (CSs), the phonotaxis of female Acheta domesticus ranges from being very selective to unselective. Within 15 min of nanoinjecting juvenile hormone III (JHIII) or picrotoxin (PTX) into the prothoracic ganglion, females become more selective for syllable period (SP) than in pre‐tests. Controls for JHIII experiments, including nanoinjection of acetone into the prothoracic ganglion or nanoinjection of JHIII into the metathoracic ganglion, do not influence selectivity. Similarly, nanoinjection of saline into the prothoracic ganglion and nanoinjection of PTX outside of the prothoracic ganglion does not change the overall selectivity of the female’s phonotaxis. These results indicate that circuits in the prothoracic ganglion modulate the SP‐selectivity of phonotaxis. Photoinactivating both of the ON1 prothoracic auditory interneurones in old females that were previously unselective for SP also results in greater SP‐selectivity during phonotaxis. Evidence suggesting that ON1 has this effect via its inhibitory input to L3 (another prothoracic auditory neurone) includes: photoinactivation of one ON1 neurone causes angular errors in the female’s orientation to CSs at 85 dB (above the threshold of the L3), stimulation with 60 dB CSs (above the threshold of ON1 but below the threshold of L3) does not induce errors in angular orientation, inactivation of ON1 in old crickets results in greater angular errors (85 dB stimulus) than it does when ON1 is inactivated in young females, and photoinactivation of ON1 increases the firing rate of the L3 neurone.     

Sex differences in metabolic rates in field crickets and their dipteran parasitoids

Sex differences in metabolic rate (MR) can result from dimorphism in the performance of energetically demanding activities. Male crickets (Teleogryllus oceanicus) engage in costly calling and aggressive activity not performed by females. Consistent with this difference, we found higher maximal MR, factorial scope, and fat content in males than females. T. oceanicus song is also costly because it attracts the parasitoid fly Ormia ochracea. Parasitized crickets had reduced maximal MR consistent with a metabolic cost to harboring larvae. This cost was greater for females, either because females invest more heavily into reproduction at the expense of metabolic capacity, or because males are under stronger selection to respond to infection. Little is known about O. ochracea outside of its auditory system and parasitic lifestyle. We observed greater resting MR in male flies, possibly reflecting a sex difference in the requirement for metabolic power output, because male flies perform potentially costly mating behavior not seen in females. We found a positive relationship between larval density within a cricket and pupal resting MR, suggesting that crickets in good condition are able to both harbor more larvae and produce larvae with higher resting MR. These results reveal a complex interplay between the metabolism of crickets and their fly parasitoids.Communicated by G. Heldmaier