Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

The effect of temperature on male mating signals and female choice in the red mason bee,Osmia bicornis (L.)

Climate change and the resulting changes in air temperature are known to have a major influence on most animals, especially poikilothermic insects, because they depend on the high enough temperatures to function. Previous studies have shown that various signals can be affected by changes in temperature. However, research into the effect of temperature on mating signals and subsequently communication between mates and on female choice is still rare. In the red mason bee, Osmia bicornis, which emerges early in spring and is therefore subject to extensive temperature changes, females choose suitable males based on, among other criteria, their thorax vibrations and odor. So far there has been no research into the effect of temperature changes on these signals. We therefore investigated whether the environmental temperature has an influence on the male's mating signals by measuring vibrations using a laser vibrometer and collecting male and female odor at different temperatures. Furthermore, we performed behavioral experiments in order to show whether there is an effect of temperature‐induced changes and female choice. Our results showed that rejected males differed in their vibrations between the two temperature settings but accepted ones did not. Temperature changes therefore seem to have a stronger effect on those males that are rejected by the females, whereas the accepted males are the ones that can produce desirable signals despite temperature fluctuations. Furthermore, we found that the differences in odor profiles were greater between temperature settings than between the sexes and that females change their preference for odor with temperature. We conclude that temperature strongly influences the male mating signals and therefore may have a major impact on sexual selection in this species. This is an important aspect to consider, not only in future studies on mating behavior, but also in view of our ever raising temperatures.     

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.     

Information‐gathering as a response to manipulated signals in the eastern fence lizard,Sceloporus undulatus

Colorful visual signals are used across taxa to convey information during agonistic male‐male encounters, which are important for sexual selection. Although much is known about the information content of color signals, less is known about how receivers interpret this information. Here, using territorial Sceloporus undulatus lizards in a natural setting, we examined receiver response to intruders with different color patch sizes to determine (a) if patch size conveys information assessed during male‐male interactions and (b) if/how receivers modulate their behavioral responses to different types of behavioral signals. We found that larger lizards had longer and wider patches, indicating that the size of the patches may be one of the many characteristics of these patches that is used by males to convey information. Free‐ranging subject males also produced more headbob displays in response to intruders with small patches and took marginally longer to react to intruders with large patches. However, we found no differences in the aggressiveness of the response (i.e., fullshows). This indicates that patch size conveys information that is employed during territorial disputes, but that the response is primarily in terms of timing, allowing lizards to gather more information about intruders, instead of aggressive behavior (i.e., fullshows).     

Detection of female mating status using chemical signals and cues

Males of many species choose their mate according to the female's reproductive status, and there is now increasing evidence that male fitness can depend on this discrimination. However, females will also aim to regulate their mating activity so as to maximize their own fitness. As such, both sexes may attempt to dictate the frequency and timing of female mating, reflecting the potentially different costs of female signaling to both sexes. Here, I review evidence that chemical cues and signals are used widely by males to discriminate between mated and unmated females, and explore the mechanisms by which female odour changes post‐mating. There is substantial empirical evidence that mated and unmated females differ in their chemical profile, and that this variation provides males with information on a female's mating status. Although there appears to be large variation among species regarding the mechanisms by which female odour is altered post‐mating, the transfer of male substances to females during or subsequent to copulation appear to play a major role. This transfer of substances by males may be part of their strategy to suppress reproduction by competing males, particularly in species where females mate more than once.     

Population differences in the roles of size and coloration in intra-and intersexual selection in the collared lizard, Crotaphytus collaris: influence of habitat and social organization

Previous studies have shown that in three Oklahoma populationsof collared lizards, Wichita Mountains (WM), Glass Mountains(GM), and Arcadia Lake (AL), sexual dimorphism in body sizevaries as WM>AL>GM, whereas dorsal color dimorphism variesas GM>WM>AL. Social organization at these sites also differssuch that the environmental potential for sexual selection variesas AL>WM>GM. We conducted female choice and male competitionlaboratory trials to assess whether advantages to large or brightmales correlate best with the interpopulation pattern of sexualdimorphism or with that of the environmental potential for sexualselection. Between-population trials involved bright-coloredWM males and dull-colored AL males that were matched for size.AL females preferred bright WM males, but WM females did not.WM males had higher agonistic scores in intrasexual contestswhen aggression was low, but AL males consistently had higherscores when aggression escalated. Within-population trials involvedmales that were disparate in color but size matched and disparatein size but color matched. Size was important in male contestsin all populations. Color brightness was a factor in male trialsonly at AL. Also, only AL females preferred brighter males,and larger males were not preferred in any population. The importanceof intra and intersexual selection in these populations cannotbe inferred from the observed pattern of size and color dimorphism.Rather, interpopulation differences in the environmental potentialfor females to assess and choose from among multiple males,and for males to interact, are most consistent with the observedoutcomes.     

Sex differences in lizard escape decisions vary with latitude,but not sexual dimorphism

Sexual selection is a powerful evolutionary mechanism that has shaped the physiology, behaviour and morphology of the sexes to the extent that it can reduce viability while promoting traits that enhance reproductive success. Predation is one of the underlying mechanisms accounting for viability costs of sexual displays. Therefore, we should expect that individuals of the two sexes adjust their anti-predator behaviour in response to changes in predation risk. We conducted a meta-analysis of 28 studies (42 species) of sex differences in risk-taking behaviour in lizards and tested whether these differences could be explained by sexual dichromatism, by sexual size dimorphism or by latitude. Latitude was the best predictor of the interspecific heterogeneity in sex-specific behaviour. Males did not change their escape behaviour with latitude, whereas females had increasingly reduced wariness at higher latitudes. We hypothesize that this sex difference in risk-taking behaviour is linked to sex-specific environmental constraints that more strongly affect the reproductive effort of females than males. This novel latitudinal effect on sex-specific anti-predator behaviour has important implications for responses to climate change and for the relative roles of natural and sexual selection in different species.     

Lineage-specific differences in evolutionary mode in a salamander courtship pheromone

Functionally equivalent genes may evolve heterogeneously across closely related taxa as a consequence of lineage-specific selective pressures. Such disparate evolutionary modes are especially prevalent in genes that encode postcopulatory reproductive proteins, presumably as a result of sexual selection. We might therefore expect genes that mediate reproduction prior to insemination to evolve in a similar manner. Plethodontid receptivity factor (PRF), a proteinaceous salamander pheromone produced by the male, increases female receptivity during courtship interactions. To test for lineage-specific differences in PRF's evolution, we intensively sampled PRF genes across the eastern Plethodon phylogeny (27 spp.; 34 populations) to compare gene diversification, rates of evolution, modes of selection, and types of amino acid substitution. Our analyses indicate that PRF evolutionary dynamics vary considerably from lineage to lineage. Underlying this heterogeneity, however, are two well-defined transitions in evolutionary mode. The first mode is representative of a typical protein profile, wherein neutral divergence and purifying selection are the dominant features. The second mode is characterized by incessant, cyclical evolution driven by positive selection. In this mode, the positively selected sites are bound by a limited assortment of acceptable amino acids that appear to evolve independently of other sites, resulting in a tremendous number of unique PRF alleles. Several of these selected sites are implicated in receptor binding. These sites are apparently involved in a molecular tango in which the male signal and female receptors coevolve within a confined molecular space. PRF's lineage-specific evolutionary dynamics, in combination with evidence of a molecular tango, highlight the molecular action of sexual selection on a chemical signal that is used during courtship.     

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae)

Variation in temperature can affect the expression of a variety of important fitness‐related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences—as well as the relationship between how male signals and female mate preferences change across temperatures (signal–preference temperature coupling)—in Enchenopa binotata treehoppers. These small plant‐feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal–preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals—the trait for which females show strongest preference—and female peak preference—the signal frequency most preferred by females—across a range of biologically relevant temperatures (18°C–36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal–preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal–preference matches, and directional selection in those with signal–preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal–preference mismatches at thermal extremes.     

Sexual selection and experimental evolution of chemical signals in Drosophila pseudoobscura

Our expectations for the evolution of chemical signals in response to sexual selection are uncertain. How are chemical signals elaborated? Does sexual selection result in complexity of the composition or in altered quantities of expression? We addressed this in Drosophila pseudoobscura by examining male and female cuticular hydrocarbons (CHs) after 82 generations of elevated (E) sexual selection or relaxed sexual selection through monogamy (M). The CH profile consisted of 18 different components. We extracted three eigenvectors using principal component analysis that explained 72% of the variation. principal component (PC)1 described the amount of CHs produced, PC2 the trade‐off between short‐ and long‐chain CHs and PC3 the trade‐off between apparently arbitrary CHs. In both sexes, the amount of CHs produced was greater in flies from the E treatment. PC3 was also higher, indicating that sexual selection also influenced the evolution of CH composition. The sexes differed in all three PCs, indicating substantial sexual dimorphism in this species, although the magnitude of this dimorphism was not increased as a result of our experimental evolution. Collectively, our work provides direct evidence that sexual selection plays an important role in the evolution of CHs in D. pseudoobscura and that both increased quantity and overall composition are targeted.     

Relationship between pre‐ and post‐copulatory traits in Salvator rufescens (Squamata: Teiidae)

Understanding pre‐ and post‐copulatory mechanisms of sexual selection can provide insights into the evolution of male reproductive strategies. The phenotype‐linked fertility hypothesis postulates that male sperm quality and secondary sexual characteristics will positively co‐vary, whereas the sperm competition hypothesis predicts a negative association between those traits. Male reproductive traits often show variation throughout the reproductive period, suggesting that the relationship between pre‐ and post‐copulatory sexual selection may vary temporally. Here, we evaluated the relationship between secondary sexual character and sperm traits and its temporal variation in Salvator rufescens, a south American lizard. We observed a negative relationship between jaw muscle and principal piece length of sperm and a variation in the relationship between pre‐ and post‐copulatory traits throughout the reproductive period. Collectively, our results evidenced a trade‐off between pre‐ and post‐copulatory traits and a strong seasonal flexibility of male reproductive strategies in this lizard species.     

Disruption of the chemical communication of the European agrobiont ground‐dwelling spider Pardosa agrestis by pesticides

Lycosid spiders are among the most abundant and diverse insectivores occurring in all agroecosystems. Certain pest management practices, such as the application of pesticides, can disrupt their role in insect pest control. Therefore, understanding the effects of pesticides, including sublethal effects, is essential for the assessment of chemical effects on beneficial arthropods. We investigated the sexual chemical communication of the beneficial agrobiont spider Pardosa agrestis and its disruption by two widely used pesticides, the glyphosate‐based herbicide Roundup and the pyrethroïd‐based insecticide Nurelle D. A two‐choice olfactometer and Y‐maze were used to study the effectiveness of female airborne and dragline pheromone cues and the disruptive effect of the pesticides. Males of P. agrestis did not locate females via airborne cues, but were very receptive to female dragline silk and male dragline silk. When both female dragline silk and male dragline silk were provided at the same time, the males preferred female silk. Pesticide treatments significantly affected the male ability to follow female cues deposited on dragline silk. The 3‐h residues of both Roundup and Nurelle D significantly disrupted the male ability to follow female cues deposited on dragline silk. Treatment by 48‐h residues significantly disrupted the male ability only in the case of Nurelle D. Our results demonstrate that pesticides reduce the ability of male spiders to search for a mate due to the disruption of the male's ability to detect the silk cues of the female.     

The evolution of courtship display repertoire size in the dabbling ducks (Anatini)

Many animals possess multiple ornaments or behaviours that seem to have evolved via sexual selection. A complete understanding of sexual selection requires an explanation for such multiple traits. The dabbling ducks (Tribe: Anatini) exhibit considerable variation among species in the number of displays in the male courtship repertoire. I tested five hypotheses concerning the evolution of the variation in display repertoire size of dabbling ducks: (1) species recognition, (2) courtship habitat, (3) sexual selection intensity, (4) display media tradeoff and (5) time constraints on pair formation. I tested these hypotheses, using an explicit phylogenetic hypothesis developed from DNA sequences for the dabbling ducks, with two types of statistical comparative methods (discrete and continuous character). The variation observed in male courtship display repertoire size in dabbling ducks was consistent with the courtship habitat and sexual selection intensity hypotheses. Specifically, the size of the display repertoire was larger in species that exhibit courtship exclusively on water and larger in species with dimorphic plumage. These results suggest that ecological (habitat) as well as social (sexual selection) factors may be important in driving the evolution of displays in the dabbling ducks.     

Aposematism increases acoustic diversification and speciation in poison frogs

Multimodal signals facilitate communication with conspecifics during courtship, but they can also alert eavesdropper predators. Hence, signallers face two pressures: enticing partners to mate and avoiding detection by enemies. Undefended organisms with limited escape abilities are expected to minimize predator recognition over mate attraction by limiting or modifying their signalling. Alternatively, organisms with anti-predator mechanisms such as aposematism (i.e. unprofitability signalled by warning cues) might elaborate mating signals as a consequence of reduced predation. We hypothesize that calls diversified in association with aposematism. To test this, we assembled a large acoustic signal database for a diurnal lineage of aposematic and cryptic/non-defended taxa, the poison frogs. First, we showed that aposematic and non-aposematic species share similar extinction rates, and aposematic lineages diversify more and rarely revert to the non-aposematic phenotype. We then characterized mating calls based on morphological (spectral), behavioural/physiological (temporal) and environmental traits. Of these, only spectral and temporal features were associated with aposematism. We propose that with the evolution of anti-predator defences, reduced predation facilitated the diversification of vocal signals, which then became elaborated or showy via sexual selection.     

Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition

During insemination, males of internally fertilizing speciestransfer a complex array of seminal fluid proteins to the femalereproductive tract. These proteins can have profound effectson female reproductive physiology and behavior and are thoughtto mediate postcopulatory sexual selection and intersexual conflict.Such selection may cause seminal fluid to evolve rapidly, withpotentially important consequences for speciation. Here we investigatethe evolution of seminal fluid proteins in a major mammalianradiation, the muroid rodents, by quantifying diversity in seminalfluid proteome composition for the first time across a broadrange of closely related species. Using comparative proteomicstechniques to identify and cross-match proteins, we demonstratethat rodent seminal fluid is highly diverse at the level ofboth proteomes and individual proteins. The striking interspecificheterogeneity in seminal fluid composition revealed by our surveyfar exceeds that seen in a second proteome of comparable complexity,skeletal muscle, indicating that the complement of proteinsexpressed in seminal fluid may be subject to rapid diversification.We further show that orthologous seminal fluid proteins exhibitsubstantial interspecific variation in molecular mass. Becausethis variation cannot be attributed to differential glycosylationor radical differences in termination sites, it is stronglysuggestive of rapid amino acid divergence. Sperm competitionis implicated in generating such divergence for at least onemajor seminal fluid protein in our study, SVS II, which is responsiblefor copulatory plug formation via transglutaminase-catalyzedcross-linking after insemination. We show that the molecularmass of SVS II is positively correlated with relative testissize across species, which could be explained by selection foran increased number of cross-linking sites involved in the formationof the copulatory plug under sperm competition.     

Patterns of sexual dimorphism in Mexican alligator lizards,Barisia imbricata

We compare morphological characteristics of male and female Barisia imbricata, Mexican alligator lizards, and find that mass, head length, coloration, incidence of scars from conspecifics, tail loss, and frequency of bearing the color/pattern of the opposite sex are all sexually dimorphic traits. Overall size (measured as snout–vent length), on the other hand, is not different between the two sexes. We use data on bite scar frequency and fecundity to evaluate competing hypotheses regarding the selective forces driving these patterns. We contend that sexual selection, acting through male‐male competition, may favor larger mass and head size in males, whereas large females are likely favored by natural selection for greater fecundity. In addition, the frequency of opposite‐sex patterning in males versus females may indicate that the costs of agonistic interactions among males are severe enough to allow for an alternative mating strategy. Finally, we discuss how sexual and natural selective forces may interact to drive or mask the evolution of sexually dimorphic traits.