DOES LARGE BODY SIZE IN MALES EVOLVE TO FACILITATE FORCIBLE INSEMINATION? A STUDY ON GARTER SNAKES

A trend for larger males to obtain a disproportionately high number of matings, as occurs in many animal populations, typically is attributed either to female choice or success in male-male rivalry; an alternative mechanism, that larger males are better able to coercively inseminate females, has received much less attention. For example, previous studies on garter snakes (Thamnophis sirtalis parietalis) at communal dens in Manitoba have shown that the mating benefit to larger body size in males is due to size-dependent advantages in male-male rivalry. However, this previous work ignored the possibility that larger males may obtain more matings because of male-female interactions. In staged trials within outdoor arenas, larger body size enhanced male mating success regardless of whether a rival male was present. The mechanism involved was coercion rather than female choice, because mating occurred most often (and soonest) in females that were least able to resist courtship-induced hypoxic stress. Males do physically displace rivals from optimal positions in the mating ball, and larger males are better able to resist such displacement. Nonetheless, larger body size enhances male mating success even in the absence of such male-male interactions. Thus, even in mating systems where males compete physically and where larger body size confers a significant advantage in male-male competition, the actual selective force for larger body size in males may relate to forcible insemination of unreceptive females. Experimental studies are needed to determine whether the same situation occurs in other organisms in which body-size advantages have been attributed to male-male rather than male-female interactions.     

Sexual dimorphism in the tusked frog, Adelotus brevis (Anura:Myobatrachidae): the roles of natural and sexual selection

At least two adaptive processes can lead to the evolution of sexual dimorphism: sexual selection (e.g. male-male combat) or natural selection (e.g. dietary divergence). We investigated the adaptive significance of a distinctive pattern of sexual dimorphism in a south-eastern Australian frog, Adelotus brevis. Male Adelotus grow larger than female conspecifics, have larger heads relative to body size, and have large paired projections (‘tusks’) in the lower jaw. All of these traits are rare among anurans. We quantified the degree of dimorphism in Adelotus, and gathered data on diets and mating systems of this species to evaluate the possible roles of sexual selection and dietary divergence in favoring die evolution of these sexually dimorphic traits. Analysis of prey items in alimentary tracts revealed significant sex differences in prey types. For example, females ate proportionally more arthropods and fewer molluscs than did males. However, this difference is likely to be a secondary consequence of habitat differences between the sexes (due in turn to their different reproductive roles) rather than a selective force for the evolution of sexual dimorphism. Calling males spend their time in moist habitats where pondsnails are abundant, whereas females are more often encountered in the drier arthropod-rich woodlands. A three-year behavioural ecology study on a field population revealed that reproductive males engage in agonistic interactions, with the sexually dimorphic tusks used to attack rivals. Larger body size contributed to male reproductive success. Small males were excluded from calling sites and, among the calling males, larger animals had higher reproductive success (numbers of matings) than did smaller individuals. Hence, the atypical pattern of sexual dimorphism in Adelotus brevis seems to have resulted from sexual selection for larger body size and tusk size in males, in the context of male-male agonistic behaviour, rather than natural selection for ecological divergence between the sexes.     

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.     

BODY SIZE AND SEXUAL SIZE DIMORPHISM IN MARINE IGUANAS FLUCTUATE AS A RESULT OF OPPOSING NATURAL AND SEXUAL SELECTION: AN ISLAND COMPARISON

Body size is often assumed to represent the outcome of conflicting selection pressures of natural and sexual selection. Marine iguana (Amblyrhynchus cristatus) populations in the Galápagos exhibit 10-fold differences in body mass between island populations. There is also strong sexual size dimorphism, with males being about twice as heavy as females. To understand the evolutionary processes shaping body size in marine iguanas, we analyzed the selection differentials on body size in two island populations (max. male mass 900 g in Genovesa, 3500 g in Santa Fé). Factors that usually confound any evolutionary analysis of body sizes—predation, interspecific food competition, reproductive role division—are ruled out for marine iguanas. We show that, above hatchlings, mortality rates increased with body size in both sexes to the same extent. This effect was independent of individual age. The largest animals (males) of each island were the first to die once environmental conditions deteriorated (e.g., during El Niños). This sex-biased mortality was the result of sexual size dimorphism, but at the same time caused sexual size dimorphism to fluctuate. Mortality differed between seasons (selection differentials as low as –1.4) and acted on different absolute body sizes between islands. Both males and females did not cease growth when an optimal body size for survival was reached, as demonstrated by the fact that individual adult body size phenotypically increased in each population under favorable environmental conditions beyond naturally selected limits. But why did marine iguanas grow “too large” for survival? Due to lek mating, sexual selection constantly favored large body size in males (selection differentials up to +0.77). Females only need to reach a body size sufficient to produce surviving offspring. Thereafter, large body size of females was less favored by fertility selection than large size in males. Resulting from these different selection pressures on male and female size, sexual size dimorphism was mechanistically caused by the fact that females matured at an earlier age and size than males, whereafter they constantly allocated resources into eggs, which slowed growth. The observed allometric increase in sexual size dimorphism is explained by the fact that the difference between these selective processes becomes larger as energy abundance in the environment increases. Because body size is generally highly heritable, these selective processes are expected to lead to genetic differences in body size between islands. We propose a common-garden experiment to determine the influence of genetic factors and phenotypic reaction norms of final body size.     

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.     

Path analysis and the relative importance of male-female conflict, female choice and male-male competition in water striders

Three major behavioural mechanisms underlying sexual selection in many systems are male-male competition, female choice and male-female conflict. We used path analysis to evaluate the relative importance of these mechanisms in generating sexual selection on a suite of male traits in the stream-dwelling water strider, Aquarius remigis. To gather data for the analysis, we quantified the morphology (total length, limb length, forefemur width, genital length), behaviour (activity), mating frequency, mean mating duration and overall mating success of 96 adult males over a 10-day period. Males varied considerably in mating success. Over the 10 days, individual males mated 0-14 times, spending 0-67% of their time in copula. Path analysis showed that male-male competition was important in favouring larger males with longer limbs that tended to be more active. Active males should encounter females more frequently. In water striders, almost all male-female encounters result in intense premating struggles pitting female resistance to mating against male insistence. This male-female conflict favoured larger males with longer genitalia. These traits help males overcome female resistance. Female choice was expressed via female-controlled variation in mate-guarding durations. Female choice favoured smaller males perhaps because they are lighter, less expensive ‘shields’ against harassment by other males. Male size thus affected mating success via all three behavioural mechanisms. Weak, overall sexual selection favouring larger males was the product of conflicting effects: male-female conflict strongly favouring larger males and male-male competition weakly favouring larger males, offset by female choice favouring smaller males. Separate analyses for warmer versus colder days showed that on colder days (daily high below 20 °C), male-male competition was the main mechanism generating variation in mating frequency, while on warmer days, both male-male competition and male-female conflict were important. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection

Bumblebees and other eusocial bees offer a unique opportunity to analyze the evolution of body size differences between sexes. The workers, being sterile females, are not subject to selection for reproductive function and thus provide a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other natural selection. Using a phylogenetic comparative approach, we explored the allometric relationships among queens, males, and workers in 70 species of bumblebees (Bombus sp.). We found hyperallometry in thorax width for males relative to workers, indicating greater evolutionary divergence of body size in males than in sterile females. This is consistent with the hypothesis that selection for reproductive function, most probably sexual selection, has caused divergence in male size among species. The slope for males on workers was significantly steeper than that for queens on workers and the latter did not depart from isometry, providing further evidence of greater evolutionary divergence in male size than female size, and no evidence that reproductive selection has accelerated divergence of females. We did not detect significant hyperallometry when male size was regressed directly on queen size and our results thus add the genus Bombus to the increasing list of clades that have female-larger sexual size dimorphism and do not conform to Rensch's rule when analyzed according to standard methodology. Nevertheless, by using worker size as a common control, we were able to demonstrate that bumblee species do show the evolutionary pattern underlying Rensch's rule, that being correlated evolution of body size in males and females, but with greater evolutionary divergence in males.     

Male aggressive behavior and exaggerated hindlegs of the bean bug Riptortus pedestris

Males of the bean bug species Riptortus pedestris possess larger hindlegs than females. Observations of male-male interactions showed that the enlarged hindlegs are used as weapons in male fights, and that males with larger hindlegs win fights more frequently. Morphological analysis based on the positive allometry test showed that the femora of larger males are relatively bigger than those of smaller males, but femora of larger females are not relatively larger than those of smaller females. These results suggest that sexual selection in R. pedestris favors larger hindlegs for male fighting. In addition, the thorax and abdomen lengths were larger in the male than in the female. The males often lift their abdomen with their back to the opponent for displays against an opponent. As a result, abdominal size may be under stronger selection in the male than in the female, as for the exaggerated hindlegs.     

Opposing selection on a sexually dimorphic trait through female choice and male competition in a water boatman

Female choice and male-male competition are traditionally considered to act in concert, with male competition facilitating female choice. This situation would enforce the strength of directional selection, which could reduce genetic variation and thus the benefits of choice. Here I show that in a water boatman, Sigara falleni, the direction of selection through female choice and male competition vary among traits under laboratory conditions. The two forces were mutually enforcive in acting on body size but exerted opposing selection on a sexually selected trait, male foreleg pala size. Female choice favored large palae, whereas male competition favored smaller palae, suggesting that large palae are costly in competition. This conflicting selection through female choice and male competition could be one of the forces that contribute to the maintenance of genetic variation in sexually selected traits.     

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.     

Factors driving extreme sexual size dimorphism of a sit-and-wait predator under low density

Sexual size dimorphism is often a likely outcome of the interplay between natural selection and sexual selection, with female size dictated primarily by natural selection that maximizes fecundity and male size by sexual selection that maximizes reproductive opportunities. Attention to male fitness has focused heavily on direct male-male conflict selecting for superior male size and/or fighting ability, although male reproductive traits vary immensely among animals. An alternative, advanced by Michael Ghiselin, posits highly mobile dwarf males as a strategy for finding relatively immobile females in low-density populations. Adult male crab spiders Misumena vatia , sit-and-wait predators, are strikingly smaller, much more active, and relatively longer-legged than their females. This size difference results largely from males having two fewer instars than females, which simultaneously results in marked protandry. Populations of M. vatia often were small and of low density, with a female-biased sex ratio and an operational sex ratio that changed strikingly over the season. Sexual selection through scramble competition (locating the female first) should favour this suite of characters in males of low-density populations. Although direct male-male contests favoured large males, the low densities of adult males and the dispersed, relatively immobile females led to low levels of direct intrasexual contest. Females exaggerated the problem of males in finding them by providing few cues to their presence, a pattern consistent with indirect mate choice. In addition to favouring high mobility, scramble competition favoured males that selected flowers attracting many prey, the sites most often occupied by females.     

The relationship between male head size and harem size in the sexually dimorphic mountain stone weta Hemideina maori

Abstract 1. Tree weta are a group of large, flightless orthopterans with pronounced sexual dimorphism. Males have enlarged heads that are used in fighting for possession of cavities in trees or under rocks where females shelter during the day.
2. The fieldwork reported here examined the relationship between male head size and mating success in Hemideina maori , an alpine tree weta that shelters under rock slabs that have broken off isolated outcrops or tors.
3. The relationship between male head size and harem size in H. maori is not as clear-cut as thought previously. First, overall body size is a better predictor of male mating success than head size per se . Second, both body size and head size explained a relatively low percentage (19.8%) of the overall variation in mating success. Third, despite the intensity of directional selection being estimated to move the frequency distribution of head size and femur size 0.49 and 0.54 standard deviations from the mean, male heads and femurs were ≈ 2 mm smaller at the main study site than at a second site 100 m higher in elevation. A similar pattern was found for adult females. Additional surveys have indicated that body size in H. maori decreases with decreasing altitude, which is correlated with increasing night-time temperature.
4. Although there are reasons why natural selection might favour weta maturing earlier and at smaller body sizes in warmer environments, relatively large males would still have a mating advantage over smaller males under such conditions. This sexually dimorphic alpine insect might be a good example of the trade-offs and conflicting demands that sexual selection versus natural selection can place on organisms.     

Sex identification and mating in the blue-ringed octopus, Hapalochlaena lunulata

We studied the reproductive behaviour of the blue-ringed octopus, Hapalochlaena lunulata, in the laboratory by examining 15 male-male and nine male-female interactions. The initiation of physical contact was independent of sex, size or residency status, and there were no noticeable changes in behaviour such as sexual displays associated with courtship or aggression prior to contact. Males did not distinguish between females or other males and copulated (defined as the insertion of the hectocotylus into the mantle cavity of another octopus) readily with both. Spermatophores were released in all copulations with females but not with males. The duration of copulation was significantly longer in male-female interactions (median 160.5 min) than in male-male interactions (median 30 s). Although male-male copulations ended passively with the withdrawal of the hectocotylus by the initiating animal, male-female copulations were always terminated by the females following an intense struggle. These studies suggest the inability of male H. lunulata to determine the sexual identity of potential mates prior to the insertion of the hectocotylus and demonstrate the active role of the female during copulation. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sexually antagonistic coevolution in insects is associated with only limited morphological diversity

Morphological traits involved in male-female sexual interactions, such as male genitalia, often show rapid divergent evolution. This widespread evolutionary pattern could result from sustained sexually antagonistic coevolution, or from other types of selection such as female choice or selection for species isolation. I reviewed the extensive but under-utilized taxonomic literature on a selected subset of insects, in which male-female conflict has apparently resulted in antagonistic coevolution in males and females. I checked the sexual morphology of groups comprising 500-1000 species in six orders for three evolutionary trends predicted by the sexually antagonistic coevolution hypothesis: males with species-specific differences and elaborate morphology in structures that grasp or perforate females in sexual contexts; corresponding female structures with apparently coevolved species-specific morphology; and potentially defensive designs of female morphology. The expectation was that the predictions were especially likely to be fulfilled in these groups. A largely qualitative overview revealed several surprising patterns: sexually antagonistic coevolution is associated with frequent, relatively weak species-specific differences in males, but male designs are usually relatively simple and conservative (in contrast to the diverse and elaborate designs common in male structures specialized to contact and hold females in other species, and also in weapons such as horns and pincers used in intra-specific battles); coevolutionary divergence of females is not common; and defensive female divergence is very uncommon. No cases were found of female defensive devices that can be facultatively deployed. Coevolutionary morphological races may have occurred between males and females of some bugs with traumatic insemination, but apparently as a result of female attempts to control fertilization, rather than to reduce the physical damage and infections resulting from insertion of the male's hypodermic genitalia. In sum, the sexually antagonistic coevolution that probably occurs in these groups has generally not resulted in rapid, sustained evolutionary divergence in male and female external sexual morphology. Several limitations of this study, and directions for further analyses are discussed.     

Influence of male morphology on male mating status and behavior during interunit encounters in western lowland gorillas

The western lowland gorilla (Gorilla gorilla gorilla) is one of the most sexually dimorphic primate species. Mature males are twice the size of females and have grey fur on their backs and a fibrous, adipose crest on their heads. Such traits are likely to have evolved by sexual selection, either because they confer advantages during male-male fights or because females prefer males with more dimorphic traits. We developed photogrammetric methods for distance collection of morphological data from silverback males frequenting the Lokoué forest clearing in Odzala-Kokoua National Park, Republic of the Congo. Body length, head-crest size, musculature development, and extent of the grey color on the back were assessed in 87 nonbreeding and breeding mature males. Behavioral data were also collected during 312 male-male encounters involving 67 mature males in order to estimate their level of aggressiveness. The number of females belonging to a mature male positively correlated with the male crest size, body length, and musculature. Whereas morphological variables did not significantly affect the intensity of male-male encounters, the number of females attending male-male encounters strongly affected the number of agonistic displays by the two males. We discuss the mechanisms through which males with more exaggerated traits could obtain a mating advantage, namely male-male fights or female mate choice.     

BREEDING COMPETITION IN A PACIFIC SALMON (COHO: ONCORHYNCHUS KISUTCH): MEASURES OF NATURAL AND SEXUAL SELECTION

In the breeding system of Pacific salmon, females compete for oviposition territories, and males compete to fertilize eggs. The natural selection in females and sexual selection in males likely has been responsible for their elaborate breeding morphologies and the dimorphism between the sexes. We quantified direct-selection intensities during breeding on mature coho salmon (Oncorhynchus kisutch), measured for seven phenotypic characters, including three secondary sexual characters. Wild and sea-ranched hatchery coho were used to enhance the range of phenotypes over which selection could be examined. The fish were allowed to breed in experimental arenas where we could quantify components of breeding success as well as estimate overall breeding success. We found that without competition, natural selection acts only on female body size for increased egg production; there is no detectable selection on males for the phenotypic distribution we used. Under competition, the opportunity for selection increased sixfold among females. Natural selection favored female body size and caudal-peduncle (tail) depth. Increased body size meant increased egg production and access to nesting territories. The caudal peduncle, used in burst swimming and nest digging, influenced both successful egg deposition and nest survival. Increasing density increased competition among females, though it did not significantly intensify natural selection on their characters. In males, competition increased the opportunity for selection 52-fold, which was nine times greater than for females. Sexual selection favored male body size and hooked snout length, both characters directly influencing male access to spawning opportunities. Selection on male body size was also affected significantly by breeding density. The ability of large males to control access to spawning females decreased at higher densities reflecting an increase in the operational sex ratio. Further, the relative success of small males, which could sneak access to spawning females, appeared to increase as that of intermediate-sized males decreased. Such disruptive selection may be responsible for the evolution of alternative reproductive tactics in salmon.     

Does ‘gliding while gravid’ explain Rensch's rule in flying lizards?

Among species with sexual size dimorphism (SSD), taxa in which males are the larger sex have increasing SSD with increasing body size, whereas in taxa in which females are the larger sex, SSD decreases with body size: Rensch's rule. We show in flying lizards, a clade of mostly female‐larger species, that SSD increases with body size, a pattern similar to that in clades with male‐biased SSD or more evenly mixed SSD. The observed pattern in Draco appears due to SSD increasing with evolutionary changes in male body size; specifically divergence in body size among species that are in sympatric congeneric assemblages. We suggest that increasing body size, resulting in decreased gliding performance, reduces the relative gliding cost of gravidity in females, and switches sexual selection in males away from a small‐male, gliding advantage and toward selection on large size and fighting ability as seen in many other lizards. Thus, selection for large females is likely greater than selection for large males at the smaller end of the body size continuum, whereas this relationship reverses for species at the larger end of the continuum. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 270–282.     

Male-male competition and large size mating advantage in European earwigs, Forficula auricularia

European earwigs are sexually dimorphic in forceps shape and length. Male forceps are thought to be weapons in male contests for access to females, but recent findings suggest that females choose males on the basis of their forceps length. I investigated sexual selection on forceps length and body size and the occurrence of male-male competition. When I controlled for forceps length experimentally and statistically, relatively heavy males had greater copulation success than relatively light males. When I controlled for body size, males with relatively longer forceps had no tendency for greater copulation success than males with shorter forceps. Relatively heavy males more often took over copulations from smaller males than vice versa. Male contests were important for the outcome of mate competition, as males commonly interrupted and took over copulations. My results therefore suggest that intrasexual selection is significant in competition for copulations in male earwigs, and acts on body size. This contrasts with previous findings, which have shown intersexual selection on forceps length to be important. However, both modes of sexual selection may be acting through a two-stage process, where male-male competition first determines which males have access to females, and then through female choice among available males. Morphological measurements supported the conclusion that forceps length and body size are male secondary sexual characters, as these characters had large variance and skewed distributions in males, but were normally distributed in females. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sexual selection, antennae length and the mating advantage of large males in Asellus aquaticus

In crustacean species with precopulatory mate-guarding, sexual size dimorphism has most often been regarded as the consequence of a large male advantage in contest competition for access to females. However, large body size in males may also be favoured indirectly through scramble competition. This might partly be the case if the actual target of selection is a morphological character, closely correlated with body size, involved in the detection of receptive females. We studied sexual selection on body size and antennae length in natural populations of Asellus aquaticus, an isopod species with precopulatory mate guarding. In this species, males are larger than females and male pairing success is positively related to body size. However, males also have longer antennae, relative to body size, than females, suggesting that this character may also be favoured by sexual selection. We used multivariate analysis of selection to assess the relative influences of body size and antennae length in five different populations in the field. Selection gradients indicated that, overall, body size was a better predictor of male pairing success than antennae length, although some variation was observed between sites. We then manipulated male antennae length in a series of experiments conducted in the lab, and compared the pairing ability of males with short or long antennae. Males with short antennae were less likely to detect, orient to, and to pair with a receptive female compared with males with long antennae. We discuss the implications of our results for studies of male body size and sexual dimorphism in relation to sexual selection in crustaceans.     

Sexual selection, antennae length and the mating advantage of large males in Asellus aquaticus

In crustacean species with precopulatory mate-guarding, sexual size dimorphism has most often been regarded as the consequence of a large male advantage in contest competition for access to females. However, large body size in males may also be favoured indirectly through scramble competition. This might partly be the case if the actual target of selection is a morphological character, closely correlated with body size, involved in the detection of receptive females. We studied sexual selection on body size and antennae length in natural populations of Asellus aquaticus, an isopod species with precopulatory mate guarding. In this species, males are larger than females and male pairing success is positively related to body size. However, males also have longer antennae, relative to body size, than females, suggesting that this character may also be favoured by sexual selection. We used multivariate analysis of selection to assess the relative influences of body size and antennae length in five different populations in the field. Selection gradients indicated that overall body size was a better predictor of male pairing success than antennae length, although some variation was observed between sites. We then manipulated male antennae length in a series of experiments conducted in the laboratory, and compared the pairing ability of males with short or long antennae. Males with short antennae were less likely to detect, orient to and to pair with a receptive female compared to males with long antennae. We discuss the implications of our results for studies of male body size and sexual dimorphism in relation to sexual selection in crustaceans.