A multivariate view of the evolution of sexual dimorphism

Sexual differences are often dramatic and widespread across taxa. Their extravagance and ubiquity can be puzzling because the common underlying genome of males and females is expected to impede rather than foster phenotypic divergence. Widespread dimorphism, despite a shared genome, may be more readily explained by considering the multivariate, rather than univariate, framework governing the evolution of sexual dimorphism. In the univariate formulation, differences in genetic variances and a low intersexual genetic correlation () can facilitate the evolution of sexual dimorphism. However, studies that have analysed sex‐specific differences in heritabilities or genetic variances do not always find significant differences. Furthermore, many of the reported estimates of are very high and positive. When monomorphic heritabilities and a high are present together, the evolution of sexual dimorphism on a trait‐by‐trait basis is severely constrained. By contrast, the multivariate formulation has greater generality and more flexibility. Although the number of multivariate sexual dimorphism studies is low, almost all support sex‐specific differences in the G (variance‐covariance) matrix; G matrices can differ with respect to size and/or orientation, affecting the response to selection differently between the sexes. Second, whereas positive values of the univariate quantity only hinder positive changes in sexual dimorphism, positive covariances in the intersexual covariance B matrix can either help or hinder. Similarly, the handful of studies reporting B matrices indicate that it is often asymmetric, so that B can affect the evolution of single traits differently between the sexes. Multivariate approaches typically demonstrate that genetic covariances among traits can strongly constrain trait evolution when compared with univariate approaches. By contrast, in the evolution of sexual dimorphism, a multivariate view potentially reveals more opportunities for sexual dimorphism to evolve by considering the effect sex‐specific selection has on sex‐specific G matrices and an asymmetric B matrix.     

Condition-dependent signaling affects male sexual attractiveness in field crickets, Gryllus campestris

The condition dependence of sexually selected traits is an importantassumption of sexual selection theory. Several laboratory studieshave documented a positive relationship between food availability,body condition, and sexual display. However, these studies mightnot reflect the resource allocation between body maintenance,reserves, and the sexually selected trait under natural conditions.Further, the effect of condition-dependent signaling on femalemate choice has hardly been investigated experimentally in thefield. We therefore investigated the effect of food availabilityon body condition, calling behavior, and sexual attractivenessof male field crickets, Gryllus campestris, under field conditions.Food availability was manipulated for individual males by supplementingfood in a confined area close to the burrow. Food-supplementedmales showed a significant increase in body condition, whereasthe opposite was found in the control males. Males receivingextra food called more frequently, whereas the calling-songcharacteristics were not affected by the treatment. Further,food-supplemented males attracted more females than did controlmales, and their higher attractiveness was partly explainedby their superior calling rate. Our study thus indicates condition-dependentsignaling as an important determinant of the sexual attractivenessof males to females under natural condition.     

Gene duplication in the evolution of sexual dimorphism

Males and females share most of the same genes, so selection in one sex will typically produce a correlated response in the other sex. Yet, the sexes have evolved to differ in a multitude of behavioral, morphological, and physiological traits. How did this sexual dimorphism evolve despite the presence of a common underlying genome? We investigated the potential role of gene duplication in the evolution of sexual dimorphism. Because duplication events provide extra genetic material, the sexes each might use this redundancy to facilitate sex‐specific gene expression, permitting the evolution of dimorphism. We investigated this hypothesis at the genome‐wide level in Drosophila melanogaster, using the presence of sex‐biased expression as a proxy for the sex‐specific specialization of gene function. We expected that if sexually antagonistic selection is a potent force acting upon individual genes, duplication will result in paralog families whose members differ in sex‐biased expression. Gene members of the same duplicate family can have different expression patterns in males versus females. In particular, duplicate pairs containing a male‐biased gene are found more frequently than expected, in agreement with previous studies. Furthermore, when the singleton ortholog is unbiased, duplication appears to allow one of the paralog copies to acquire male‐biased expression. Conversely, female‐biased expression is not common among duplicates; fewer duplicate genes are expressed in the female‐soma and ovaries than in the male‐soma and testes. Expression divergence exists more in older than in younger duplicates pairs, but expression divergence does not correlate with protein sequence divergence. Finally, genomic proximity may have an effect on whether paralogs differ in sex‐biased expression. We conclude that the data are consistent with a role of gene duplication in fostering male‐biased, but not female‐biased, gene expression, thereby aiding the evolution of sexual dimorphism.     

Social isolation increases male aggression toward females in the field cricket Gryllus bimaculatus

Social isolation has often been reported to facilitate male aggressiveness in various animal species. If social isolation also escalates male aggressive behavior towards females, the mating success of the aggressive males will be low. This study evaluated the effect of social isolation on mating behavior in the field cricket Gryllus bimaculatus, which has traditionally been considered to be an asocial species. The results showed that social isolation from same-sex individuals enhanced male aggressiveness to females, and the mating success of aggressive males was reduced under the experimental conditions. More aggressive males exhibited a longer latency to court than less aggressive males. These results suggest that because male aggressiveness causes a delay in courtship, aggressive males may have reduced mating success. This demonstrated that social relationships are a critical factor affecting male mating success, even if the species is normally considered solitary.     

Courtship song and immune function in the field cricket Gryllus bimaculatus

It has been assumed that sexual ornaments have evolved to reveal males' health and vigour for females. Choosy females may indirectly use ornaments as an indicator of the presence and effectiveness of genes for resistance against parasites. In this study we tested whether females of the Mediterranean field cricket, Gryllus bimaculatus, can use courtship song as a cue for choosing males with high immunocompetence, measured as encapsulation rate of nylon implants and lytic activity of haemolymph. We found that female crickets preferred courtship songs from males with a high encapsulation rate. Female crickets also had a tendency to prefer courtship songs with high tick rate and long high-frequency tick duration. These preferred song components were positively correlated with encapsulation rate, but negatively correlated with lytic activity of the male. In contrast to previous studies of crickets, there was no correlation between male weight and encapsulation rate or lytic activity. There is some evidence in another cricket species that the ability to encapsulate pathogens is heritable. Thus, in light of this study it seems possible that by preferring males according to their courtship song, females might benefit by increasing the parasite resistance of their offspring.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 503–510.     

Courtship and copulation, but not ejaculates, reduce the longevity of female field crickets (Gryllus bimaculatus)

Females of many taxa incur fitness costs from male sexual coercion and harassment leading to mating. Although male crickets cannot force copulations on females, female Gryllus bimaculatus in this study incurred significant reductions in longevity through being exposed to different levels of male courtship. Virgin females kept in isolation had the longest life spans. Reductions in longevity applied to females in sensory contact with males (without the opportunity to mate), females that courted and mated and females that mated but with fertilization being prevented. Females also incurred significant reductions in longevity when kept with other females, which may have been due to high levels of cannibalism. Consistent with previous studies, females appeared to incur no cost to longevity from receiving sperm or seminal fluid. It is known that female G. bimaculatus benefit genetically from multiple mating. However, this benefit could possibly be offset by the negative effect that male courtship and mating behaviour has on female longevity.     

Costs of an induced immune response on sexual display and longevity in field crickets

Immune system activation may benefit hosts by generating resistance to parasites. However, natural resources are usually limited, causing a trade-off between the investment in immunity and that in other life-history or sexually selected traits. Despite its importance for the evolution of host defense, state-dependent fitness costs of immunity received little attention under natural conditions. In a field experiment we manipulated the nutritional condition of male field crickets Gryllus campestris and subsequently investigated the effect of an induced immune response through inoculation of bacterial lipopolysaccharides. Immune system activation caused a condition-dependent reduction in body condition, which was proportional to the condition-gain during the preceding food-supplementation period. Independent of nutritional condition, the immune insult induced an enduring reduction in daily calling rate, whereas control-injected males fully regained their baseline level of sexual signaling following a temporary decline. Since daily calling rate affects female mate choice under natural conditions, this suggests a decline in male mating success as a cost of induced immunity. Food supplementation enhanced male life span, whereas the immune insult reduced longevity, independent of nutritional status. Thus, immune system activation ultimately curtails male fitness due to a combined decline in sexual display and life span. Our field study thus indicates a key role for fitness costs of induced immunity in the evolution of host defense. In particular, costs expressed in sexually selected traits might warrant the honest advertisement of male health status, thus representing an important mechanism in parasite-mediated sexual selection.     

Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae)

Because homologous traits of males and females are likely to have a common genetic basis, sex-specific selection (often resulting from sexual selection on one sex) may generate an evolutionary tug-of-war known as intralocus sexual conflict, which will constrain the adaptive divergence of the sexes. Theory suggests that intralocus sexual conflict can be mitigated through reduction of the intersexual genetic correlation (rMF), predicting negative covariation between rMF and sexual dimorphism. In addition, recent work showed that selection should favor reduced expression of alleles inherited from the opposite-sex parent (intersexual inheritance) in traits subject to intralocus sexual conflict. For traits under sexual selection in males, this should be manifested either in reduced maternal heritability or, when conflict is severe, in reduced heritability through the opposite-sex parent in offspring of both sexes. However, because we do not know how far these hypothesized evolutionary responses can actually proceed, the importance of intralocus sexual conflict as a long-term constraint on adaptive evolution remains unclear. In this study, we investigated the genetic architecture of sexual and nonsexual morphological traits in Prochyliza xanthostoma. The lowest rMF and greatest dimorphism were exhibited by two sexual traits (head length and antenna length) and, among all traits, the degree of sexual dimorphism was correlated negatively with rMF. Moreover, sexual traits exhibited reduced maternal heritabilities, and the most strongly dimorphic sexual trait (antenna length) was heritable only through the same-sex parent in offspring of both sexes. Our results support theory and suggest that intralocus sexual conflict can be resolved substantially by genomic adaptation. Further work is required to identify the proximate mechanisms underlying these patterns.     

Sexual antagonism and the evolution of X chromosome inactivation

In most female mammals, one of the two X chromosomes is inactivated early in embryogenesis. Expression of most genes on this chromosome is shut down, and the inactive state is maintained throughout life in all somatic cells. It is generally believed that X-inactivation evolved as a means of achieving equal gene expression in males and females (dosage compensation). Following degeneration of genes on the Y chromosome, gene expression on X chromosomes in males and females is upregulated. This results in closer to optimal gene expression in males, but deleterious overexpression in females. In response, selection is proposed to favor inactivation of one of the X chromosomes in females, restoring optimal gene expression. Here, we make a first attempt at shedding light on this intricate process from a population genetic perspective, elucidating the sexually antagonistic selective forces involved. We derive conditions for the process to work and analyze evolutionary stability of the system. The implications of our results are discussed in the light of empirical findings and a recently proposed alternative hypothesis for the evolution of X-inactivation.     

Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females

Stronger selection on males has the potential to lower the deleterious mutation load of females, reducing the cost of sex. However, few studies have directly quantified the strength of selection for both sexes. As the magnitude of inbreeding depression (ID) is related to the strength of selection, we measured the cost of inbreeding for both males and females in a laboratory population of Drosophila melanogaster. Using a novel technique for inbreeding, we found significant ID for both juvenile viability and adult fitness in both sexes. The genetic variation responsible for this depression in fitness appeared to be recessive for adult fitness (h=0.11) and partially additive for juvenile viability (h=0.29). ID was identical across the sexes in terms of juvenile viability but was significantly more deleterious for males than females as adults, even though female X-chromosome homogamety should predispose them to a higher inbreeding load. We estimated the strength of selection on adult males to be 1.24 greater than on adult females, and this appears to be a consequence of selection arising from competition for mates. Combined with the generally positive intersexual genetic correlation for inbred lines, our results suggest that the mutation load of sexual females could be meaningfully reduced by stronger selection acting on males.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

Changes in the biochemical composition of fat body stores during adult development of female crickets, Gryllus bimaculatus

Age-dependent changes in the fat body composition and aspects of lipogenesis in the free abdominal fat body of female crickets, Gryllus bimaculatus, were studied. Lipid, protein, glycogen, and free carbohydrate content of the fat body, and fat body wet weight increased simultaneously and sharply from day 0 onwards and were doubled/almost doubled by day 2 after adult emergence. Lipogenic activity of the fat body, fat body weight, and the energy stores in the fat body peaked on day 2, except for free carbohydrate, which peaked on day 3. On day 2, the fat body was mainly comprised of lipid (53.8%) and protein (6.6%), while glycogen and free carbohydrate together contributed less than 1% of the fat body wet weight. After peaking, both lipogenesis and energy stores decreased in a synchronous manner. The depletion of the fat body energy stores and the consequent decrease in the fat body weight were concomitant with a fast and massive gain in ovary weight (day 2: 19.5 +/- 1.5 mg; day 4: 332.8 +/- 31.5 mg) due to the vitellogenic oocyte growth that started on day 2. Our data clearly underline the importance of the free abdominal fat body as a source of energy for reproduction in the cricket. Fat body fatty acid synthase activity coincided with lipogenic activity. Adipokinetic hormone inhibits lipid synthesis in the fat body, but treatment of the fat body with adipokinetic hormone in vitro showed no consistent effect on fatty acid synthase activity.     

Production of chitin and chitosan from the exoskeleton of adult two‐spotted field crickets (Gryllus bimaculatus)

Chitin and chitosan were extracted from all specimens of Type I and II two‐spotted field crickets (Gryllus bimaculatus) following chemical treatment with an acid and alkali. For chitin extraction, 2 N HCl and 1.25 N NaOH solutions were used to achieve demineralization and deproteinization, respectively. For chitosan extraction, 50 % NaOH (w/v) and 50 % NaOH (w/w) solutions were used to achieve deacetylation. Chitosan yielded from adult exoskeletons of G. bimaculatus in Test A of Type I was 1.76 and 8.40 % on a fresh weight (FW) and dry weight (DW) basis, respectively, after treatment with 50 % NaOH (w/v) at 95°C for 3 h. Furthermore, the chitosan yielded in Test D of Type II was 1.79 and 7.06 % on FW and DW basis, respectively, after treatment with 50 % NaOH (w/w) at 105°C for 3 h. The average yield of chitin and chitosan was 2.42 and 1.65 % on a FW basis, and 10.91 and 7.50 % on DW basis, respectively. The deacetylation (%) of chitosan extracted from adult exoskeletons in Tests A, B, C1, C2, D1, and D2 were 81.2 %, 14.5 %, 19.6 %, 90.7 %, 17.1 %, and 95.5 %, respectively. The viscosities of the chitosans extracted from adult exoskeletons in Tests A, C2, and D2 were 32.0, 21.6, and 62.4 cP (centi Poise), respectively. The molecular weight of chitosan from adult exoskeletons of G. bimaculatus was 308.3 kDa. Our results indicate that adult exoskeletons of G. bimaculatus could be used as a source of chitin and chitosan for use as functional additives in industrial animal feeds.     

Impact of motor activity and antennal mechanosensory input on the intensity of proctolin-like immunoreactivity in antennal motoneurons of crickets (Gryllus bimaculatus)

The change of the intensity of proctolin immunolabeling of 2 of 17 proctolinergic antennal motoneurons [one adductor (Ad3), and one depressor (D5)] was quantitatively studied in crickets in relation to flight and antennal deafferentation. During flight, the maintained forward position of the antennae is supported by high frequency tonic firing of Ad3 but probably all motoneurons are activated. In animals sacrificed immediately after the last of five consecutive flight periods the intensity of proctolin-like immunolabeling showed a significant decrease in the Ad3 soma in comparison to the Ad3 of non-flyers. The identical result was observed in the D5 soma. In animals sacrificed 40 h after flight, no difference in the intensity of proctolin immunolabeling between the Ad3 soma of flyers and non-flyers was evident. Thus, at high motoneuron activity, the production of proctolin may not be able to keep pace with its transport from the soma. Deletion of all proprioceptors of one antenna which respond to horizontal movements only led to a significant decrease of the intensity of proctolin immunolabeling in the Ad3 soma on the operated side, but not in the soma of D5. This indicates that selected afferent input has an impact on proctolin expression in distinct motoneuron pools. Accepted: 7 February 1997     

The contribution of multiple mating and spermatophore consumption to the lifetime reproductive success of female field crickets (Gryllus bimaculatus)

ABSTRACT.

• 1 The adaptive significance of multiple mating by female Gryllus bimaculatus (De Geer) was investigated.
• 2 Multiple mating prevented the depletion of sperm stores and, therefore, maintained high hatching success. This may not, however, explain the high frequency of remating in this species.
• 3 Male-derived egg stimulants known to be passed with sperm at mating increased the number of eggs produced only when females mated throughout their lifespans.
• 4 Spermatophore consumption appeared to provide nutrients which, while they did not increase the quantity of eggs, increased egg quality as indicated by weight. Females who consumed spermatophores had a greater hatching success.
• 5 While females may derive non-genetic benefits from mating, these are apparently long-term benefits; females must mate throughout their lives in order to accrue them.
• 6 Since the benefits of mating may not be derived from individual males, the spermatophores and their contents in this species are best considered as mating effort.

     

Testing the correlated response hypothesis for the evolution and maintenance of male mating preferences in Drosophila serrata

Mate preferences are abundant throughout the animal kingdom with female preferences receiving the most empirical and theoretical attention. Although recent work has acknowledged the existence of male mate preferences, whether they have evolved and are maintained as a direct result of selection on males or indirectly as a genetically correlated response to selection for female choice remains an open question. Using the native Australian species Drosophila serrata in which mutual mate choice occurs for a suite of contact pheromones (cuticular hydrocarbons or CHCs), we empirically test key predictions of the correlated response hypothesis. First, within the context of a quantitative genetic breeding design, we estimated the degree to which the trait values favoured by male and female choice are similar both phenotypically and genetically. The direction of sexual selection on male and female CHCs differed statistically, and the trait combinations that maximized male and female mating success were not genetically correlated, suggesting that male and female preferences target genetically different signals. Second, despite detecting significant genetic variance in female preferences, we found no evidence for genetic variance in male preferences and, as a consequence, no detectable correlation between male and female mating preferences. Combined, these findings are inconsistent with the idea that male mate choice in D. serrata is simply a correlated response to female choice. Our results suggest that male and female preferences are genetically distinct traits in this species and may therefore have arisen via different evolutionary processes.     

Weak relationships of parasite infection with sexual and life‐history traits in wild‐caught Texas field crickets (Gryllus texensis)

1. Sex differences in immune investment and infection rate are predicted due to the divergent life histories of males and females, where females invest more toward immunity due to the fitness consequences of a reduced lifespan and males allocate less toward immunity due to increased resource investment in traits critical to sexual selection. Consequently, males are expected to fight infection less adeptly, resulting in higher parasite loads relative to females across all taxa.
2. Wild animals rarely face a single parasite within their given environment, yet nearly all studies on sex‐biased infection rates have focused on a single host–parasite relationship. Here, we investigate how simultaneous natural infections of ecto‐ and endosymbionts (i.e. both parasitic and phoretic taxa) correlate with sex biases in host immune response and reproductive investment in a field‐caught cricket, Gryllus texensis.
3. Our comprehensive analysis found no significant sex differences in two measures of immune response (melanization and nodulation), and found no strong evidence of a sex bias in the prevalence or intensity of parasitism by the three most common parasites infecting wild G. texensis field crickets (Eutrombidiidae, gregarines, and nematodes).
4. Two traits related to female fitness, egg number and egg size, showed no relation to parasitic infection; however, males having wider heads and poorer body condition were significantly more infected by eutrombidiid mites, gregarines, and nematodes.
5. Despite frequent predictions of male‐biased parasitism in the literature, our results concur with many other studies indicating that the divergent life histories of males and females alone are not sufficient to explain natural infection rates in wild insects.

     

Effects of the corpora allata on sexual receptivity and completion of oocyte development in females of the cricket, Gryllus bimaculatus

Abstract Allatectomy of young penultimate nymphs of Gryllus bimaculatus De Geer (Gryllidae) resulted in prothetelic creatures which exhibited reproductive competence. The same operation performed on young last instar nymphs resulted in moulting to morphologically normal adults. Allatectomized morphologically normal adult females, as well as prothetelic ones, showed the same level of sexual receptivity as untreated control females. Allatectomized morphologically normal and prothetelic females laid viable eggs, but rate of egg laying and number of eggs produced by these females were much reduced in comparison with the controls. Administration of methoprene (a Juvenile Hormone analogue) to allatectomized females restored egg production to a more or less normal rate. Removal of the spermatophore within 10 min of copulation had no effect on subsequent sexual receptivity of the females, nor on the reduced rate of egg laying by the allatectomized females, but did affect the rate of egg laying by control females.
It is suggested that the corpora allata (CA) and the Juvenile Hormone (JH) play no major role in controlling basic sexual receptivity of G.bimaculatus females, and do not have an all-encompassing control on egg production, though they do exert a marked quantitative effect on the rate of egg production.     

Genetic interactions controlling sex and color establish the potential for sexual conflict in Lake Malawi cichlid fishes

Sex-determining systems may evolve rapidly and contribute to lineage diversification. In fact, recent work has suggested an integral role of sex chromosome evolution in models of speciation. We use quantitative trait loci analysis of restriction site-associated DNA -tag single nucleotide polymorphisms to identify multiple loci responsible for sex determination and reproductively adaptive color phenotypes in Lake Malawi cichlids. We detect a complex epistatic sex system consisting of a major female heterogametic ZW locus on chromosome 5, two separate male heterogametic XY loci on chromosome 7, and two additional interacting loci on chromosomes 3 and 20. Our data support the known chromosomal linkage between orange blotch color and ZW, as well as novel genetic associations between male blue nuptial color and two sex determining regions (an XY and ZW locus). These results provide further empirical evidence for a complex antagonistic sex–color system in this species flock and suggest a possible role for, and effect of, polygenic sex-determining systems in rapid evolutionary diversification.