Sexual size dimorphism and sexual selection in turtles (order testudines)

Summary This paper combines published and original data on sexual size dimorphism, reproductive behavior, and habitat types in turtles. Our major finding is that observed patterns of sexual size dimorphism correlate with habitat type and male mating strategy. (1) In most terrestrial species, males engage in combat with each other. Males typically grow larger than females. (2) In semiaquatic and bottom-walking aquatic species, male combat is less common, but males often forcibly inseminate females. As in terrestrial species, males are usually larger than females. (3) In truly aquatic species, male combat and forcible insemination are rare. Instead, males utilize elaborate precoital displays, and female choice is highly important. Males are usually smaller than females.We interpret these correlations between sexual behavior and size dimorphism in terms of sexual selection theory: males are larger than females when large male size evolves as an adaptation to increase success in male combat, or to enable forcible insemination of females. In contrast, males are usually smaller than females where small size in males evolves to increase mobility (and hence, ability to locate females), or because selection for increased fecundity may result in increased female size. In turtle species with male combat or forcible insemination, the degree of male size superiority increases with mean species body size.     

Effects of sex-ratio manipulation on territoriality and spawning success of male pupfish,Cyprinodon pecosensis

The sex ratio of Cyprinodon pecosensis was manipulated by varying the number of females but not of males. This resulted in some subordinate males changing their breeding tactics from satellites to territorials. The spawning success of breeding males was directly related, and the intensity of male-male competition was inversely related, to the number of available females. Time-budget data indicated a tradeoff between courtship and agonistic behaviour. In the male-biased treatment, males engaged in a greater number of agonistic interactions and fewer courtship bouts; conversely, in the female-biased treatment courtship behaviour was more frequent than aggression. A greater proportion of males adopted the satellite breeding tactic in the male-biased and even-sex-ratio treatments. Smaller, competitively inferior males were most sensitive to changes in the sex ratio. In the female-biased treatment, with an increase in mating opportunities and a decrease in the level of male-male competition for females, average mating success increased, more males were able to defend territories, and some satellite individuals were able to adopt the territorial breeding tactic. Temporal or spatial changes in the operational sex ratio of a population may have profound effects on the dynamics of the breeding system by affecting (1) the proportion of males adopting primary and secondary breeding tactics, (2) variance in reproductive success, and (3) intensity of sexual selection.     

Lekking Behaviour and Male-Male Rivalry in the Melon Fly <Emphasis Type="Italic">Bactrocera cucurbitae</Emphasis> (Coquillett) (Diptera: Tephritidae)

Most studies on the sexual behaviour of tephritid fruit flies are conducted in laboratory or field cage settings. Here, we present field data on the mating behaviour of the melon fly, Bactrocera cucurbitae (Coquillett). A number of Tephritidae are lekking species, forming aggregations in which males fight to defend a small territory where they court females and mate. Our results confirm that males of the melon flies congregated and engaged in wing vibration in the late afternoon on non-host plants, such as Ficus carica, Cydonia oblonga and Prunus persica which bordered cucurbit fields. The nature and outcome of male-male aggressive encounters are described, and a high degree of female mate selectivity is documented.     

Male-male interactions and their influence on the mating behavior and success in the fountain darter, <Emphasis Type="Italic">Etheostoma fonticola</Emphasis>

Behavioral interactions between individuals of the same sex can affect the outcome of intersexual selection. For this reason, intrasexual selection is oftentimes examined independently from intersexual selection in studies aimed at understanding mating behaviors. However, a more complete understanding of sexual selection effects within a population can only come from exploring both intrasexual and intersexual selection and the potential interactions between the levels of selection. Association preferences in male and female Etheostoma fonticola do not reveal a size preference for same sex or opposite-sex individuals. However, male-male interactions may influence female choice in E. fonticola. We examined whether male E. fonticola that differ in body size exhibit differences in agonistic behaviors and mating success. Larger males do exhibit higher rates of aggressive behaviors and smaller males, in turn, exhibit more defensive behaviors. However, differences between larger and smaller males in male-male interactions did not translate into differences in spawning success. These results suggest that male size influences dominance relationships in E. fonticola but not mating success. There were also no differences between large and small males in mating attempts, which could be an outcome of the year-round breeding season found in this species, females laying eggs singly, or males fertilizing eggs individually.     

Sexual conflict and antagonistic coevolution across water strider populations

Microevolutionary studies have demonstrated sexually antagonistic selection on sexual traits, and existing evidence supports a macroevolutionary pattern of sexually antagonistic coevolution. Two current questions are how antagonistic selection within-populations scales to divergence among populations, and to what extent intraspecific divergence matches species-level patterns. To address these questions, we conducted an intraspecific comparative study of sexual armaments and mating behaviors in a water strider (Gerris incognitus) in which male genitals grasp resistant females and female abdominal structures help ward off males. The degree of exaggeration of these armaments coevolves across species. We found a similar strong pattern of antagonistic coevolution among populations, suggesting that sexual conflict drives population differentiation in morphology. Furthermore, relative exaggeration in armaments was closely related to mating outcomes in a common environment. Interestingly, the effect of armaments on mating was mediated by population sexual size dimorphism. When females had a large size advantage, mating activity was low and independent of armaments, but when males had a relative size advantage, mating activity depended on which sex had relatively exaggerated armaments. Thus, a strong signal of sexually antagonistic coevolution is apparent even among populations. These results open opportunities to understand links between sexual arms races, ecological variation, and reproductive isolation.     

The post-copulation withdrawal response in female baboons: A functional analysis

Rapid withdrawal of females from males at the end of the copulatory sequence (prior to male dismounting) characterizes several primate species. The purpose of this paper is to make a preliminary investigation into possible functional aspects of these “copulatory darts.” Two hypotheses are proposed; (1) females use darts to aid competing males to locate the source of copulation calls; and (2) females dart in order to promote re-mating with the same male. Both hypotheses postulate that darts may thus enhance male-male competition, although acquisition of other benefits may be the primary drive to darting according to the re-mating hypothesis. Using data from 157 copulations collected from six females spread across four groups in a wild population of chacma baboonsPapio cynocephalus ursinus, darting behaviour is described. Within females, darting distance is highly variable. Darting distance is greatest at the time of ovulation (and maximal sexual swelling), and there is some evidence that darting may also be more frequent, and cover greater distances, when the mating male is adult rather than juvenile. While darting behaviour appears unrelated to the presence or absence of ejaculation, it tends to correlate positively with the duration of the female copulation call. These preliminary results are consistent with a mediating role in male-male competition and therefore provide support for both hypotheses.     

No female mate choice in Mallee dragon lizards, Ctenophorus fordi

Aspects of sexual selection were studied in a sexually monomorphic Australian agamid lizard (Ctenophorus fordi), in particular with respect to the sensory exploitation hypothesis. In enclosure trials, females were offered the choice between large vs. small males and, in a different experiment, males with blue vs. normal head color. The rationale for these experiments was: firstly, to establish if females actively solicit copulations; secondly, if so, do females solicit copulations non-randomly with respect to male size (because large males may have access to food resources); thirdly, if male coloration is manipulated to match traits of congeneric, conspicuous and sexually dimorphic species, do females show preference for this novel trait (in accordance with the sensory exploitation hypothesis). The corresponding manipulations were also made in a free-living population where the distribution of females on the home ranges of color-manipulated males were monitored. Blue-headed males were accepted as mating partners both in the staged mating trials and in the natural population. Females appeared not to express any kind of active or passive mate choice (rejection); in only one out of 62 trials did a female approach a male herself rather than being approached by the male(s). There was no discrimination against any male category regardless of size or color within a female's receptive period and the manipulation of male head color in the natural population did not result in spatial re-distribution of females. Thus, a female appears to mate unselectively within her receptive period. Rejection behaviors were used only outside of the receptive period to communicate, to all males, that the female is not receptive.     

Investigating the Consistency of Mate-Locating Behavior in the Territorial Butterfly Hypolimnas bolina (Lepidoptera: Nymphalidae)

The study of butterfly behavior has afforded valuable insights into the evolution of alternative mating tactics. Two hypotheses derived from this area of research contend that (1) territoriality is only viable under low to moderate conspecific densities (due to the costs of site defence) and (2) perching may be employed only when thermal conditions constrain flight activity. These hypotheses were evaluated by investigating mate locating behavior in Hypolimnas bolina, a territorial species that is naturally subject to variation in population density and weather conditions. Male behavior was charted throughout the day during a period of high population density at an encounter site in tropical Australia. Perching was the primary tactic, although a small proportion of individuals patrolled nonaggressively in the afternoon. Population-level male behavior failed to support predictions drawn from either the territory economics or thermal constraint hypotheses. First, the proportion of perching males and the number of aggressive conspecific interactions (per male) increased with increasing male density at the site. Second, few males patrolled at the hottest, brightest time of day (approximately midday), and the diel distribution of perchers did not emulate the U-shaped distribution shown by the occurrence of dorsal basking behavior. These results show that perching in this species is not a suboptimal tactic employed when temperatures constrain flight activity but may represent the best method of locating receptive females. At this stage the reproductive significance of the observed patrolling behavior remains obscure.     

The potential for sexual selection in males: Effect of sex ratio and spatiotemporal distribution of receptive females

Summary An animal mating system characterized by male-male competition and active searching for sexually receptive females was modelled to study how varying sex ratio and spatiotemporal distribution of receptive females can affect the variance in male mating success (i. e. potential for sexual selection) in males. The temporal distribution of female receptivity periods appeared to be the variable that had the most pronounced effect on the potential for sexual selection in males. The potential for sexual selection increased monotonically as the degree of asynchrony of female reproduction increased. Female spatial distribution and sex ratio were important only when female reproduction was asynchronous. Then, the potential for sexual selection in males was at its peak when females were overdispersed in space and the sex ratio was female biased. Some of the results derived from the model analysis contrast with predictions from previous studies. The deviating results are most likely caused by different assumptions about modes of mate acquisition in males.     

Cost of reproduction in male medflies: The primacy of sexual courting in extreme longevity reduction

In polygynous insect species, male reproductive success is directly related to lifetime mating success. However, the costs for males of sexual activities such as courting, signaling, and mating are largely unknown. We studied the cost of sexual activities in male Mediterranean fruit flies, Ceratitis capitata (Tephritidae), a polygynous lekking species, by keeping cohorts of individual male flies under relaxed crowding conditions in the laboratory. We used 5 cohorts among which individuals differed in their opportunities to interact with con-specifics and recorded life span, and in one treatment, mating rate. We found that males kept singly lived more than twice as long as males that interacted intensively with mature virgin females, while male-male interactions caused a smaller reduction in longevity. Because longevity of males that could court but not mate was not significantly different from those that could court and mate, we conclude that courting (not mating) was responsible for the observed longevity reduction. Moreover, we detected high variability in male mating success, when 5 virgin females were offered daily. In contrast to the cohort level, individual males that mated at a high rate lived relatively long, thus indicating heterogeneity in quality or sexual strategy among males.     

Sexual cannibalism in the fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints

Several hypotheses have been proposed for the evolution of sexual cannibalism by females. Newman and Elgar (1991) suggested that sexual cannibalism prior to mating by virgin female spiders may have evolved as a result of female foraging considerations. According to this model, an adult female's decision to mate or cannibalize a courting male should be based on an assessment of the male's value as a meal versus his value as a mate. The current study provides an empirical test of the assumptions and predictions of this model in the sexually cannibalistic fishing spider. Adult females were subjected to different food treatments, and exposed to adult males in the laboratory. However, only one of the assumptions of the model and none of its five predictions were upheld. We failed to find any effects of female foraging, female mating status, female size, male size or time of the season on females' behaviour towards courting males. Females behaved stereotypically, and many females were left unmated despite numerous mating opportunities. We also demonstrate costs of sexual cannibalism in a natural population. We propose that the act of sexual cannibalism in the fishing spider is non-adaptive, and develop a model for the evolution of premating sexual cannibalism in spiders based on genetic constraints. According to this hypothesis, sexual cannibalism by adult females may have evolved as an indirect result of selection for high and non-discriminate aggression during previous ontogenetic stages. Genetic covariance between different components of aggressive behaviour may constrain the degree to which (1) juvenile and adult aggression and/or (2) aggression towards conspecifics and heterospecifics can vary independently. We briefly review the support for our model, and suggest several critical tests that may be used to assess the assumptions and predictions of the model.     

Sexual dimorphism in canine length of woolly spider monkeys (Brachyteles arachnoides,E. Geoffroy 1806)

We measured canine teeth from 28 woolly spider monkeys (Brachyteles arachnoides) to assess sexual dimorphism and population differences. The specimens are from the Brazilian states of Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro, and São Paulo. We found strong sexual dimorphism in canine length for individuals belonging to populations south of 22°00 latitude but no sexual dimorphism in canine length from individuals of populations north of 21°00 latitude. Canine length did not vary among females of northern and southern populations. However, southern males had significantly longer canines than northern males. This geographical difference in canine morphology, together with the presence or absence of thumbs and published accounts of differences in genetics and social structure between northern and southern populations, suggests thatBrachyteles arachnoides may be composed of at least two subspecies, which appear to be separated by the rivers Grande and Paraiba do Sul and the Serra da Mantiqueira.     

Do Male Cook Strait Giant Weta Prudently Allocate Sperm?

Sperm production is costly and so males are expected to prudently allocate sperm to matings in a manner that maximizes their fitness. Sperm competition hypotheses predict that when facing increased sperm competition risk males should increase their investment in ejaculates. In contrast, when facing high future mating opportunities, males are expected to decrease their sperm investment in the current mating. This is because males should keep in reserve an amount of sperm proportional to their expected future mating opportunities. We experimentally tested whether male Cook Strait giant weta (Anostostomatidae: Orthoptera: Deinacrida rugosa) phenotypically adjust their investment in ejaculates in relation to their perceived risk of sperm competition and future mating opportunities. D. rugosa is a large flightless orthopteran insect in which males pass multiple spermatophores to females during a day-long mating bout. Contrary to expectation, we found that low female availability (i.e. increased sperm competition risk) had no effect on male resource allocation to sperm (i.e. number of spermatophores) compared to controls whereas, contrary to expectation, males experiencing high female availability increased their ejaculate investment by transferring significantly more spermatophores to their mates. Our results might be a consequence of males being insensitive to increased presence of rival males, reducing their allocation to sperm under increasingly risky circumstances, or due to females prolonging copulations when their perceived future mating opportunities are low.     

Behavioral and physiological female responses to male sex ratio bias in a pond-breeding amphibian

Introduction

The phenomenon of sexual conflict has been well documented, and in populations with biased operational sex ratios the consequences for the rarer sex can be severe. Females are typically a limited resource and males often evolve aggressive mating behaviors, which can improve individual fitness for the male while negatively impacting female condition and fitness. In response, females can adjust their behavior to minimize exposure to aggressive mating tactics or minimize the costs of mating harassment. While male-male competition is common in amphibian mating systems, little is known about the consequences or responses of females. The red-spotted newt (Notophthalmus viridescens) is a common pond-breeding amphibian with a complex, well-studied mating system where males aggressively court females. Breeding populations across much of its range have male-biased sex ratios and we predicted that female newts would have behavioral mechanisms to mitigate mating pressure from males. We conducted four experiments examining the costs and behavioral responses of female N. viridescens exposed to a male-biased environment.

Results

In field enclosures, we found that female newts exposed to a male-biased environment during the five-month breeding season ended with lower body condition compared to those in a female-biased environment. Shorter-term exposure to a male-biased environment for five weeks caused a decrease in circulating total leukocyte and lymphocyte abundance in blood, which suggests females experienced physiological stress. In behavioral experiments, we found that females were more agitated in the presence of male chemical cues and females in a male-biased environment spent more time in refuge than those in a female-biased environment.

Conclusions

Our results indicate that male-biased conditions can incur costs to females of decreased condition and potentially increased risk of infection. However, we found that females can also alter their behavior and microhabitat use under a male-biased sex ratio. Consistent with surveys showing reduced detection probabilities for females, our research suggests that females avoid male encounters using edge and substrate habitat. Our work illustrates the integrated suite of impacts that sexual conflict can have on the structure and ecology of a population.     

Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis

Various hypotheses have been proposed to account for the functionof sexual swellings in female primates, but few empirical dataexist to test predictions arising from these hypotheses. Controversyhas recently arisen over a field study that appeared to supportthe predictions of the reliable indicator hypothesis. This hypothesisproposes that females compete for males or matings, that differencesin swelling size between females reliably advertise female quality,and that males use swelling characteristics to differentiallyallocate mating effort to females with certain swelling characteristics,hence to females of higher quality. To provide an independenttest of this hypothesis, we collected data concerning the sizeand coloration of 40 sexual swellings for 29 semi-free-rangingfemale mandrills, varying in age and parity, along with dataconcerning the behavior of males toward the females, and comparedthese with the long-term reproductive history of the females.We examined the following predictions: (1) swelling characteristicsare consistent across subsequent cycles for individual females,(2) swelling characteristics indicate aspects of female reproductivequality, and (3) males prefer to mate with females that showparticular swelling characteristics. Our results support prediction1; we found little change in swelling characteristics acrossswellings for individual females. However, we found no significantrelationships between female reproductive history and swellingcharacteristics and, thus, no support for prediction 2. Finally,we found only limited support for prediction 3; females withlarger (wider) sexual swellings were more likely to have a spermplug when maximally swollen. However, male mate-guarding wasnot significantly related to female swelling characteristics.Furthermore, in situations in which more than one female wasmaximally swollen, the alpha male (who has "free" choice) didnot show the most interest in the female with the largest swelling.We conclude that the reliable indicator hypothesis does notexplain variation in sexual swellings in female mandrills.     

Visual acuity in larval zebrafish: behavior and histology

Background

Mating plugs that males place onto the female genital tract are generally assumed to prevent remating with other males. Mating plugs are usually explained as a consequence of male-male competition in multiply mating species. Here, we investigated whether mating plugs also have collateral effects on female fitness. These effects are negative when plugging reduces female mating rate below an optimum. However, plugging may also be positive when plugging prevents excessive forced mating and keeps mating rate closer to a females' optimum. Here, we studied these consequences in the gonochoristic nematode Caenorhabditis remanei. We employed a new CO₂-sedation technique to interrupt matings before or after the production of a plug. We then measured mating rate, attractiveness and offspring number.

Results

The presence of a mating plug did not affect mating rate or attractiveness to roving males. Instead, females with mating plugs produced more offspring than females without copulatory plugs.

Conclusions

Our experiment suggests that plugging might have evolved under male-male competition but represents a poor protection against competing males in our experiment. Even if plugging does not reduce mating rate, our results indicate that females may benefit from being plugged in a different sense than remating prevention.     

Assortative Mating by Size in the American Rubyspot Damselfly (<Emphasis Type="Italic">Hetaerina americana</Emphasis>)

Assortative mating refers to the non-random nature of mating patterns between certain males and females. Thus, males and females may associate negative- or positively, based on different traits. Amongst these associations, assortative mating by size is one of the most common patterns found in natural populations of animals. Two main hypotheses have been proposed to account for the occurrence of assortative mating by size. First, it may be the result of mechanical, temporal, or physiological constraints. Second, it may occur in response to direct or indirect selection on mating preferences. Here we investigate whether the American rubyspot damselfly exhibits true assortative mating by size. Males of this species exhibit high levels of male-male competition, as they compete over territories, to which females are attracted for copulation. There is a documented large male body size advantage: the largest males are better able to hold their territories and thus secure more copulations. Our major results show that i) mated males are more likely to be larger than unmated males, whereas mated and unmated females tend to have similar body sizes; ii) H. americana exhibits true assortative mating by size; as such, this pattern is not driven by seasonal changes in the body sizes of males and females. We suggest that this mating pattern occurs in this species given the advantages of large male size, and the advantages of large female body size (i.e. higher fecundity). We believe that males may be able to evaluate a female’s reproductive value and exert mate choice.     

Competing dwarf males: sexual selection in an orb-weaving spider

Hypotheses for the adaptive significance of extreme female-biased sexual size dimorphism (SSD) generally assume that in dimorphic species males rarely interfere with each other. Here we provide the first multivariate examination of sexual selection because of male-male competition over access to females in a species with 'dwarf' males, the orb-weaving spider Argiope aurantia. Male A. aurantia typically try to mate opportunistically during the female's final moult when she is defenceless. We show that, contrary to previous hypotheses, the local operational sex ratio (males per female on the web) is male-biased most of the season. Both interference and scramble competition occur during opportunistic mating, the former leading to significant selection for large male body size. Male condition and leg length had no effect on mating success independent of size. We discuss these findings in the context of the evolution of extreme female-biased SSD in this clade.     

Sexual cannibalism, competition, and size dimorphism in the orb-weaving spider Nephila plumipes Latreille (Araneae: Araneoidea)

The degree and direction of sexual dimorphism varies widely,but in several taxa of orb-weaving spiders, including Nephila,males may be less than one-tenth the size of females. This differenceis commonly attributed to selection through precopulation sexualcannibalism: females may either fail to detect very small males,or ignore them as potential prey items. However, there is oftenthe potential for male-male competition in these species becauseseveral males can be found on the web of a single female. Weinvestigated experimentally the effects of sexual cannibalismand male-male competition on male body size and hence sexualdimorphism in the Australian golden orb-weaver (Nephila plumipes).Small males were less likely to be detected and cannibalizedthan larger males. However, larger males excluded small malesfrom the central hub of the web, where mating takes place. Theconflicting effects of sexual cannibalism and male-male competitionmay be responsible for the relatively large variation in malebody size in this species.     

Male age and sexual experience affect male mating behavior in the hawthorn spider mite,Amphitetranychus viennensis

As is reported, in species with first-male sperm precedence, male age and previous sexual experience play crucial roles in male mating behavior. In the hawthorn spider mite, Amphitetranychus viennensis Zacher, previous studies showed that only females that copulated for the first time could achieve fertilization. Based on this, the effects of male age and mating history on male mate choice and male mate competition were investigated. It was confirmed that males could distinguish virgins from fertilized females but they were unable to discriminate between virgins and unfertilized females. Interestingly, the copulation duration of males mated with fertilized females was much shorter than that of males mated with virgins or unfertilized females. Additionally, for male mating choice, males of all ages and more experienced males preferred 5-day-old virgin females, whereas only less experienced males preferred 1-day-old virgin females. In male-male competition, 3-day-old males were more competitive and obtained more copulations compared with others. Copula duration was closely related to male age. Though no significant differences were observed in mating competition between virgin and mated males, copula duration of males in first copulation was the longest and gradually shortened in subsequent copulations. In all, this investigation demonstrated that male age and sexual experience affected male mate choice and male-male competition, leading to further insight into the influences of male age and sexual experience on the reproductive fitness of both sexes.