Genetic variation underlying the expression of a polyphenism

Polyphenic traits are widespread and represent a conditional strategy sensitive to environmental cues. The environmentally cued threshold (ET) model considers the switchpoint between alternative phenotypes as a polygenic quantitative trait with normally distributed variation. However, the genetic variation for switchpoints has rarely been explored empirically. Here, we used inbred lines to investigate the genetic variation for the switchpoint in the mite Rhizoglyphus echinopus, in which males are either fighters or scramblers. The conditionality of male dimorphism varied among inbred lines, indicating that there was genetic variation for switchpoints in the base population, as predicted by the ET model. Our results also suggest a mixture between canalized and conditional strategists in R. echinopus. We propose that major genes that canalize morph expression and affect the extent to which a trait can be conditionally expressed could be a feature of the genetic architecture of threshold traits in other taxa.     

Sexual selection for male mobility in a giant insect with female-biased size dimorphism

Female-biased size dimorphism, in which females are larger than males, is prevalent in many animals. Several hypotheses have been developed to explain this pattern of dimorphism. One of these hypotheses, the mobility hypothesis, suggests that female-biased size dimorphism arises because smaller males are favored in scramble competition for mates. Using radiotelemetry, we assessed the mobility hypothesis in the Cook Strait giant weta (Deinacrida rugosa), a species with strong female-biased size dimorphism, and tested the prediction that male traits promoting mobility (i.e., longer legs, smaller bodies) are useful in scramble competition for mates and thus promote reproductive success. Our predictions were supported: males with longer legs and smaller bodies exhibited greater mobility (daily linear displacement when not mating), and more mobile males had greater insemination success. No phenotypic traits predicted female mobility or insemination success. In species with female-biased size dimorphism, sexual selection on males is often considered to be weak compared to species in which males are large or possess weaponry. We found that male giant weta experience sexual selection intensities on par with males of a closely related harem-defending polygynous species, likely because of strong scramble competition with other males.     

Sex‐specific plasticity and genotype × sex interactions for age and size of maturity in the sheepshead swordtail,Xiphophorus birchmanni

Responses to sexually antagonistic selection are thought to be constrained by the shared genetic architecture of homologous male and female traits. Accordingly, adaptive sexual dimorphism depends on mechanisms such as genotype‐by‐sex interaction (G×S) and sex‐specific plasticity to alleviate this constraint. We tested these mechanisms in a population of Xiphophorus birchmanni (sheepshead swordtail), where the intensity of male competition is expected to mediate intersexual conflict over age and size at maturity. Combining quantitative genetics with density manipulations and analysis of sex ratio variation, we confirm that maturation traits are dimorphic and heritable, but also subject to large G×S. Although cross‐sex genetic correlations are close to zero, suggesting sex‐linked genes with important effects on growth and maturation are likely segregating in this population, we found less evidence of sex‐specific adaptive plasticity. At high density, there was a weak trend towards later and smaller maturation in both sexes. Effects of sex ratio were stronger and putatively adaptive in males but not in females. Males delay maturation in the presence of mature rivals, resulting in larger adult size with subsequent benefit to competitive ability. However, females also delay maturation in male‐biased groups, incurring a loss of reproductive lifespan without apparent benefit. Thus, in highly competitive environments, female fitness may be limited by the lack of sex‐specific plasticity. More generally, assuming that selection does act antagonistically on male and female maturation traits in the wild, our results demonstrate that genetic architecture of homologous traits can ease a major constraint on the evolution of adaptive dimorphism.     

Maternal and paternal contributions to egg size and egg number variation in the blackfin pearl killifish <Emphasis Type="Italic">Austrolebias nigripinnis</Emphasis>

Reproductive effort, egg number and egg size are traditionally considered to be ‘female’ life history traits. However, females often adjust the amount of resources allocated to reproduction depending on their mate, causing male environmental effects on life history traits. If females respond to male traits which are genetically variable, then male environmental effects contain indirect genetic effects. Estimates of how much of the total variation in life history traits originates from female effects versus male environmental effects, seems mostly lacking. We have investigated variation in rates of egg production and in egg size in the annual Argentinian blackfin pearl killifish Austrolebias nigripinnis, in a crossed design where males were exchanged repeatedly between females. Our analysis of phenotypic variance components of reproductive effort, egg size and egg number indicates that the amount of variation contributed by male environmental effects is equal (egg size, reproductive effort) or larger (egg number) than that between females. For egg size and number, we find that male environmental effects consist of a male random effect representing the average response of females to male phenotype, plus a female-male interaction term. This term can be understood as the deviation from the population mean of an individual female’s response. For reproductive effort, we find that the male environmental effect consists of an interaction term only. Random effects on egg size and number additionally vary in magnitude depending on the weekday where we collected eggs, probably due to cyclic variation in experimental conditions. Since we find that both male phenotype and environmental conditions affect egg size and number as determined by females, our results suggest that selection on these life history traits will be frequency-dependent.     

Sexual variation in assimilation efficiency: its link to phenotype and potential role in sexual dimorphism

Sex-specific variation in morphology (sexual dimorphism) is a prevalent phenomenon among animals, and both dietary intake and resource allocation strategies influence sexually dimorphic traits (e.g., body size or composition). However, we investigated whether assimilation efficiency (AE), an intermediate step between dietary intake and allocation, can also vary between the sexes. Specifically, we tested whether sex-based differences in AE can explain variation in phenotypic traits. We measured morphometric characteristics (i.e., body length, mass, condition, and musculature) and AE of total energy, crude protein, and crude fat in post-reproductive adult Children’s pythons (which exhibit a limited female-biased sexual size dimorphism) fed both low and high dietary intakes. Meal size was negatively related to AE of energy. Notably, male snakes absorbed crude protein more efficiently and increased epaxial (dorsal) musculature faster than females, which demonstrates a link between AE and phenotype. However, females grew in body length faster but did not absorb any nutrient more efficiently than males. Although our results do not provide a direct link between AE and sexual size dimorphism, they demonstrate that sexual variation in nutrient absorption exists and can contribute to other types of sex-based differences in phenotype (i.e., sexual dimorphism in growth of musculature). Hence, testing the broader applicability of AE’s role in sexually dimorphic traits among other species is warranted.     

Estimating sexual dimorphism by method-of-moments

Estimating the degree of sexual dimorphism is difficult in fossil species because most specimens lack indicators of sex. We present a procedure that estimates sexual dimorphism in samples of unknown sex using method-of-moments. We assume that the distribution of a metric trait is composed of two underlying normal distributions, one for males and one for females. We use three moments around the mean of the combined-sex distribution to estimate the means and the common standard deviation of the two underlying distributions. This procedure has advantages over previous methods: it is relatively simple to use, specimens need not be assigned to sex a priori, no reference to living species analogs is required, and the method provides conservative estimates of dimorphism under a variety of conditions. The method performs best when the male and female distributions overlap minimally but also works well when overlap is substantial. Simulations indicate that this relatively simple method is more accurate and reliable than previous methods for estimating dimorphism. © 1996 Wiley-Liss, Inc.     

Selection on male size,leg length and condition during mate search in a sexually highly dimorphic orb-weaving spider

Mate search plays a central role in hypotheses for the adaptive significance of extreme female-biased sexual size dimorphism (SSD) in animals. Spiders (Araneae) are the only free-living terrestrial taxon where extreme SSD is common. The gravity hypothesis states that small body size in males is favoured during mate search in species where males have to climb to reach females, because body length is inversely proportional to achievable speed on vertical structures. However, locomotive performance of males may also depend on relative leg length. Here we examine selection on male body size and leg length during mate search in the highly dimorphic orb-weaving spider Argiope aurantia, using a multivariate approach to distinguish selection targeted at different components of size. Further, we investigate the scaling relationships between male size and energy reserves, and the differential loss of reserves. Adult males do not feed while roving, and a size-dependent differential energy storage capacity may thus affect male performance during mate search. Contrary to predictions, large body size was favoured in one of two populations, and this was due to selection for longer legs. Male size was not under selection in the second population, but we detected direct selection for longer third legs. Males lost energy reserves during mate search, but this was independent of male size and storage capacity scaled isometrically with size. Thus, mate search is unlikely to lead to selection for small male size, but the hypothesis that relatively longer legs in male spiders reflect a search-adapted morphology is supported.     

The evolution of condition-dependent sexual dimorphism

Theory suggests that the net benefit of allocating resources to a sexual trait depends both on the strength of sexual selection on that trait and on individual condition. This predicts a tight coevolution between sexual dimorphism and condition dependence and suggests that these patterns of within-sex and between-sex variation may share a common genetic and developmental basis. Although condition-dependent expression of sexual traits is widely documented, the extent of covariation between condition dependence and sexual dimorphism remains poorly known. I investigated the effects of condition (larval diet quality) on multivariate sexual dimorphism in the fly Telostylinus angusticollis (Neriidae). Condition determined the direction of sexual size dimorphism and modulated sexual shape dimorphism by affecting allometric slopes and/or intercepts of sexually homologous traits in both sexes. Although the greatest responses to condition manipulation were observed in male sexual traits, both sexual and nonsexual traits exhibited substantial variation in the nature and magnitude of condition effects. Nonetheless, condition dependence and sexual dimorphism were remarkably congruent: variation in the strength of condition effects on male traits explained more than 90% of the variation in the magnitude of sexual dimorphism, whether quantified in terms of trait size or allometric slope. The genetic mechanisms that give rise to multivariate sexual dimorphism in body shape thus function in a strongly condition-dependent manner in this species, suggesting a common genetic basis for body shape variation within and between sexes.     

Genetic structure of Triatoma venosa (Hemiptera: Reduviidae): molecular and morphometric evidence

Triatoma venosa presents a restricted geographical distribution in America and is considered as a secondary vector of Chagas disease in Colombia and Ecuador. A total of 120 adult insects were collected in domestic and peridomestic habitats in an endemic area of the department of Boyacá, Colombia, in order to determine their genetic structure through morphometric and molecular techniques. The head and wings of each specimen were used for the analyses of size, shape, and sexual dimorphism. A significant sexual dimorphism was found, although no differences in size among the studied groups were detected. Differences were found in the analyzed structures except for male heads. DNA was extracted from the legs in order to carry out the internal transcriber space-2 (ITS-2) amplification and the randon amplified polymorphic DNA (RAPD) analyses. Length polymorphisms were not detected in the ITS-2. Fst and Nm values were estimated (0.047 and 3.4, respectively). The high genetic flow found among the insects captured in the domicile and peridomiciliary environment does not permit a genetic differentiation, thus establishing the peridomicile as an important place for epidemiological surveillance.     

Variation in cranial form and sexual dimorphism among five European populations of the otter Lutra lutra

Craniometric variation between otters Lutra lutra (L.) from Ireland, Scotland, Shetland, Norway, and Czechoslovakia was examined using multivariate statistical analyses. Significant sexual dimorphism in cranial size and shape occurred in all samples, although the degree of dimorphism varied between samples, with the Irish sample exhibiting the most. Morphological differences were also observed across samples. Three groups were observed; Irish, Scottish, (Mainland and Shetland), and Mainland European, though within the two composite groups the samples were still differentiable. There was a good agreement between the patterns of variation between male and female samples, but morphological differentiation was not significantly correlated with geographic separation. These results are discussed in the light of our current knowledge of the ecology of the species in Europe. It is argued that, while there is morphological evidence for subspecific status of the Irish otter (as L. l. roensis ), further investigations of morphological and genetic variation across Eurasia are clearly required.     

Between‐sex genetic covariance constrains the evolution of sexual dimorphism in Drosophila melanogaster

Males and females share much of their genome, and as a result, intralocus sexual conflict is generated when selection on a shared trait differs between the sexes. This conflict can be partially or entirely resolved via the evolution of sex‐specific genetic variation that allows each sex to approach, or possibly achieve, its optimum phenotype, thereby generating sexual dimorphism. However, shared genetic variation between the sexes can impose constraints on the independent expression of a shared trait in males and females, hindering the evolution of sexual dimorphism. Here, we examine genetic constraints on the evolution of sexual dimorphism in Drosophila melanogaster cuticular hydrocarbon (CHC) expression. We use the extended G matrix, which includes the between‐sex genetic covariances that constitute the B matrix, to compare genetic constraints on two sets of CHC traits that differ in the extent of their sexual dimorphism. We find significant genetic constraints on the evolution of further dimorphism in the least dimorphic traits, but no such constraints for the most dimorphic traits. We also show that the genetic constraints on the least dimorphic CHCs are asymmetrical between the sexes. Our results suggest that there is evidence both for resolved and ongoing sexual conflict in D. melanogaster CHC profiles.     

Sexual dimorphism in leg length among orb-weaving spiders: a possible role for sexual cannibalism

The degree and direction of sexual dimorphism across different species is commonly attributed to differences in the selection pressures acting on males and females. The extent of these differences is especially apparent in species that practise sexual cannibalism, where the female attempts to capture and eat a courting male. Here, we investigate the relationship between sexual dimorphism in size and leg length, sexual cannibalism and courtship behaviour in three taxonomic groups of orb-weaving spiders, using morphological data from 249 species in 36 genera. Females are larger than males in all three taxonomic groups, and males have relatively longer legs than females in both the Araneinae and Tetragnathidae. Across genera within each taxonomic group, male body size is positively correlated with both female body size and male leg length, and female body size is positively correlated with female leg length. Sexual size dimorphism is negatively correlated with relative male leg length within the Araneinae, but not within either the Tetragnathidae or the Gasteracanthinae. There was no negative correlation between sexual size dimorphism and relative female leg length in any taxonomic group. We argue that the relationship between sexual size dimorphism and relative male leg length within the Araneinae may be the result of selection imposed by sexual cannibalism by females.     

The B-matrix harbors significant and sex-specific constraints on the evolution of multicharacter sexual dimorphism

The extent to which sexual dimorphism can evolve within a population depends on an interaction between sexually divergent selection and constraints imposed by a genetic architecture that is shared between males and females. The degree of constraint within a population is normally inferred from the intersexual genetic correlation, r(mf) . However, such bivariate correlations ignore the potential constraining effect of genetic covariances between other sexually coexpressed traits. Using the fruit fly Drosophila serrata, a species that exhibits mutual mate preference for blends of homologous contact pheromones, we tested the impact of between-sex between-trait genetic covariances using an extended version of the genetic variance-covariance matrix, G, that includes Lande's (1980) between-sex covariance matrix, B. We find that including B greatly reduces the degree to which male and female traits are predicted to diverge in the face of divergent phenotypic selection. However, the degree to which B alters the response to selection differs between the sexes. The overall rate of male trait evolution is predicted to decline, but its direction remains relatively unchanged, whereas the opposite is found for females. We emphasize the importance of considering the B-matrix in microevolutionary studies of constraint on the evolution of sexual dimorphism.     

THE EVOLUTION OF ALTERNATE MORPHOLOGIES: FITNESS AND WING MORPHOLOGY IN MALE SAND CRICKETS

Many organisms show distinct morphological types. We argue that the evolution of these alternate morphologies depends upon both fitness differences between morphs within each sex and the genetic correlation between sexes. In this paper, we examine the evolution of alternate morphologies using wing dimorphism in insects as a model system. Many insect species are wing dimorphic, one morph having wings and being capable of flight, the other lacking functional wings. While there is a well established trade-off in females between macroptery and reproduction, there are few data on the possible costs in males. We examine trade-offs between macroptery and life-history traits in male sand crickets, Gryllus firmus, and estimate the genetic correlation of wing dimorphism between the sexes. Macropterous males develop faster than micropterous males and are either larger or the same size depending upon rearing conditions. There is no difference in absolute or relative testis size at eclosion or 7 d thereafter. Finally, there is no difference between macropterous and micropterous males in relative success at siring offspring. Thus, with respect to the above traits, there are no costs associated with being winged in male G. firmus. It is possible that there may be a trade-off between calling rate and macroptery. A comparison of the relative frequency of macroptery between males and female across different orders of insects supports this hypothesis. The genetic correlation of wing dimorphism between the sexes is high (r₈ = 0.86), and hence the frequency of macroptery in males may be strongly influenced by selection acting on females.     

Sex-specific non-pheromonal taste receptors in Drosophila

Taste receptorshave recently been reported in Drosophila [1] and [2], but little is known of the relation between receptor and response. Morphological studies of the distribution of chemosensory sensilla indicate that the fruit fly has two major sites of gustation: the proboscis and the legs [3]. The taste sensilla on both these sites are similar in structure and each sensillum generally houses four gustatory neurons [4]. Early anatomical observations have demonstrated a sexual dimorphism in the number of tarsal sensilla [5] and in their central projections [6]. We measured the electrophysiological responses of the prothoracic taste sensilla to non-pheromonal substances—salts, sugars and water—and found a clear sexual dimorphism. From the response profile of individual sensilla, we were able to distinguish three types of tarsal sensilla in females as against only two types in males. The female-specific type, which responded specifically to sugar, was absent in males except when male gustatory neurons were genetically feminised. The fact that tarsal gustatory hairs exhibit a sexual dimorphism that affects the perception of non-pheromonal compounds suggests that sexual identity is more complex than has previously been thought [7] and [8].     

Effects of Social Structure on the Behaviour and Performance of Alternative Reproductive Phenotypes in Male Rock Shrimp, Rhynchocinetes typus

Males that adopt alternative mating tactics within a conditional strategy often undergo costly morphological changes when switching to the next phenotype during ontogeny. Whether costs of changing to a subsequent reproductive phenotype are outweighed by a higher mating probability may depend on the frequencies of different phenotypes in a group of competitors. Benefits and costs associated with different phenotype frequencies depend on interactions within and between alternative phenotypes, but the underlying behavioural mechanisms have rarely been studied. Herein, we used the rock shrimp Rhynchocinetes typus as a model: ontogenetic male stages of this species differ in morphological and behavioural traits that indicate alternative reproductive phenotypes. The small, subordinate, male stage (typus) develops via several intermediate stages (intermedius) to the dominant male stage (robustus): in competitive interactions the typus males usually employ the sneaking tactic, while the robustus males invariably employ the monopolizing fighter tactic. In laboratory experiments, we manipulated phenotype frequencies to examine whether there are frequency‐dependent effects on searching behaviour, aggressiveness and mating probability. With increasing frequency of robustus males, the rate of aggressive interactions among them increased. Furthermore, robustus males increased walking velocity when more than one robustus male was present. In contrast, typus males did not adjust their searching or aggressive behaviour. The increase of aggressive interactions among robustus males provided more opportunities for typus males to seize a temporarily unguarded female. While typus males exploit fights among robustus males that produce mating opportunities for them, robustus males benefit from typus males, which reveal the presence of receptive females. We suggest that each phenotype benefits from the presence of the other phenotype and suffers costly interference among individuals of the same phenotype. Whether frequency‐dependent effects on the mating probability of subordinates also affect their ontogenetic switchpoint should be examined in future studies.     

Genetic control of sexually dimorphic axon morphology in Drosophila sensory neurons

The mechanism by which orderly axonal projections are formed during development remains an important and largely unsolved problem in neurobiology. It may be possible to examine the control of axon growth in Drosophila and take advantage of genetic tools to better understand the phenomenon. We show here that some gustatory axons in Drosophila are sexually dimorphic and that genes involved in sex determination control the anatomy of these axons. Both males and females possess gustatory receptors on their legs but males possess more of these receptors than females. More significantly, the axons of the male receptors usually cross the midline and they never do so in females, indicating a central zone of bilateral input in the male but not in the female nervous system. In chromosomal females, expressing a tra or Sxl mutation, the gustatory system is transformed toward the male phenotype. Mutant XX adults resemble normal males externally, because they have more gustatory receptors, and internally, because their axons cross the midline. Gynandromorphs show that the sex of the sensory neuron, and apparently not the central nervous system, controls the growth of the axons. We conclude that the anatomical site of control for this dimorphism is the gustatory neurons.     

It is not always about body size: evidence of Rensch's rule in a male weapon

In many species, sexual dimorphism increases with body size when males are the larger sex but decreases when females are the larger sex, a macro-evolutionary pattern known as Rensch''s rule (RR). Although empirical studies usually focus exclusively on body size, Rensch''s original proposal included sexual differences in other traits, such as ornaments and weapons. Here, we used a clade of harvestmen to investigate whether two traits follow RR: body size and length of the fourth pair of legs (legs IV), which are used as weapons in male–male fights. We found that males were slightly smaller than females and body size did not follow RR, whereas legs IV were much longer in males and followed RR. We propose that sexual selection might be stronger on legs IV length than on body size in males, and we discuss the potential role of condition dependence in the emergence of RR.     

Cytogenetics of the South American Akodont rodents (Cricetidae) X. Akodon mollis: a species with XY females and B chromosomes

The morphology, G- and C-banding pattern of the Akodon mollis chromosome complement is analysed. Over a total of 14 males and 10 females studied, 8 males and 7 females had a modal chromosome number of 22, while 6 males and 3 females showed a modal number of 23 chromosomes. In the animals with 23 chromosomes the odd element was considered a B chromosome on the basis of: (a) its small size, (b) the lack of an homologous chromosome and the subsequent formation of univalents at diakinesis and metaphase I from testes, (c) the weak or null genetic action as evidenced by the lack of any obvious variation in the phenotype of carriers.Four females exhibited a sex-pair dimorphism indistinguishable from that observed in males. The G-banding analysis showed homology between the pattern found in the Y chromosome and that detected in the short arm of the X. The study of C-band distribution showed that several autosome pairs and the X chromosomes had small masses of centromeric heterochromatin. On the other hand, the Y and B chromosomes were C-band negative. The Y-like chromosome in females with dimorphism of the sex pair was also C-band negative. Accordingly these females were considered to be XY and not Xx (the x being an extensively deleted X chromosome).This work was supported by grants from UNESCO, OEA, CONICET and CIC. Requests for reprints should be addressed to N.O. Bianchi.