Post-copulatory Guarding Research Articles

Rapid diversification of male genitalia and mating strategies inOhomopterusground beetles

We analysed evolutionary diversification and covariation in male genitalia and four mating traits related to sexual selection, i.e. testis size, spermatophore size, copulation duration and post-copulatory guarding duration, in Ohomopterus ground beetles using phylogenetically independent contrasts. Male genital size and mating duration have evolved more rapidly than body size and the other traits studied. Male genital size was negatively correlated with copulation duration, suggesting that elongated male genitalia may enable decreased time investment in a single copulation because it is more effective at facilitating spermatophore deposition. Male genital size was positively correlated with spermatophore size, suggesting coevolution between offensive and defensive male mating tactics because the elongated male genitalia may be advantageous in displacement of rivals' plug-like spermatophores, and decreased mating duration may intensify sperm competition. Thus, the remarkable diversity of male genitalia in Ohomopterus may have been facilitated by the interplay between inter- and intrasexual selection processes.

Spermatophore displacement and male fertilization success in the ground beetle Carabus insulicola

Sperm displacement is an effective male mating tactic of sperm competition to ensure paternity. However, the effectiveness of sperm displacement may depend on defensive mating tactics employed by rival males and also may be affected by females. To test this hypothesis, I conducted double-mating experiments with microsatellite paternity analyses using the ground beetle Carabus insulicola. First, I examined how often spermatophore displacement by the second male occurs. Spermatophore deposition success of the second male was high (85%) as was that of the first male (100%), in which 80% of the second males displaced the first male’s spermatophore, suggesting that spermatophore displacement is a highly effective offensive tactic of sperm competition in C. insulicola. Second, I examined the effects of postcopulatory guarding by the first male and remating interval and sperm utilization pattern of the female on fertilization success of the second male. P2 values were moderate on average (0.30‐0.57) and negatively correlated with postcopulatory guarding duration of the first male. Sperm use by the female was temporally nonrandom, such that sperm of the second male tended to be used first, although there was no significant effect of female-remating interval. These results suggest that the effectiveness of spermatophore displacement depends on postcopulatory guarding by the first male and the sperm utilization pattern of the female. These findings provide empirical evidence for the conflicting nature of selection for male offensive and defensive tactics in sperm competition and significant contribution of females therein. Key words: genitalia, microsatellite, P2, sexual selection, sperm competition. [Behav Ecol]

Sperm competition promotes diversity of sperm bundles in Ohomopterus ground beetles

Diversification of sperm morphology has been investigated in the context of sperm competition, but the adaptive significance of sperm bundles is still unclear. In analyzing 10 taxa of the genus Carabus subgenus Ohomopterus and one related Carabus ground beetles, we found that dimorphic sperm bundles occurred in most species with varied degrees of bimodality, whereas sperm were generally monomorphic. Comparative analyses with phylogenetically independent contrasts revealed that the sizes of large and small sperm bundles evolved more rapidly than, and were not correlated with, the length of sperm, suggesting more intense selection on sperm bundle sizes and their independent responses to different evolutionary forces. The size of large sperm bundles was positively correlated with male genital morphology (pertinent to displacement of rival spermatophores) and postcopulatory guarding duration as well as male body length, suggesting that larger sperm bundles have been favored when the risk of spermatophore displacement is high. Larger sperm bundles may be advantageous because of their ability to migrate more rapidly into the spermatheca. In contrast, no clear association was detected between the small sperm bundle size and mating traits despite its rapid diversification. The present study provides the first record of heteromorphic sperm bundles, the diversity of which may be promoted by sperm competition.

Comparative Analysis of the Mating Strategies in Grapsid Crabs with Special References to the Intertidal Crabs Cyclograpsus Lavauxi and Helice Crassa (Decapoda: Grapsidae) from New Zealand

Field and laboratory observations were carried out on the reproductive behaviour of Cyclograpsus lavauxi and Helice crassa, and the results were compared with other Grapsidae, with emphasis on New Zealand species. Mating in all species typically occurs during the intermoult and often coincides with the time of oviposition. Females of several species have been reported to mate multiple times, often in the few days prior to oviposition, leading to sperm competition within the female spermatheca. Females were found to be sexually receptive only in a short period before oviposition (e.g., C. lavauxi, Hemigrapsus crenulatus, H. sexdentatus), although some species were also receptive for about two weeks after oviposition (e.g., H. crassa). The exact duration of female receptivity is unknown for most grapsid species. Female grapsid crabs exhibit a wide range of gonopore structures which either restrict female receptivity to certain times or allow them to mate at any time. In species with restricted female receptivity (e.g., C. lavauxi, H. crassa, H. crenulatus, H. sexdentatus), the operational sex ratio is typically highly male-biased. Male-male competition was found to be intense in the four New Zealand grapsids, with frequent male-male interactions during which larger males were typically more successful in fights over females, resulting in a greater number of matings. Postcopulatory guarding, which is assumed to reduce the risk of sperm competition and to ensure paternity, has been observed in a few grapsid species (H. sexdentatus and H. crenulatus) but not in others (e.g., C. lavauxi and H. crassa). Overall, grapsid crabs employ a variety of reproductive strategies including direct competition between males for females, with postcopulatory guarding; males securing resources as sites for mating; and males having only brief interceptions with receptive females. These differences in reproductive behaviour are discussed in the context of sexual selection and the ecological and environmental differences of the habitats that grapsid crabs occupy. Mating strategies of grapsid species can be very different even if they occupy the same habitat and the females have similar duration of sexual receptivity.

Mating behaviour, female receptivity and male–male competition in the intertidal crab Hemigrapsus sexdentatus (Brachyura: Grapsidae)

Female receptivity and male-male competition were studied in a laboratory population of the New Zealand rock crab Hemigrapsus sexdentatus. Mating only occurred in the few days prior to oviposition, when females had mobile gonopore opercula. After mating, males guarded females constantly and mated with them repeatedly until the females laid eggs. Isolated females remained receptive for significantly longer than females housed temporarily or constantly with males in the lab- oratory. The duration of female receptiveness can, therefore, vary in relation to the presence of males. Male-male competition was high with frequent attacks on pairs by other males. Large males mated significantly more often than medium and small males, and were more likely to take over a female from another male. However, large and small male H. sexdentatus both adjusted the ejaculate size according to the size of the female; i.e. transferred relatively large ejaculates to large females, and were equally able to transfer ejaculates to small and large females during the first mating in the sea- son. Post-copulatory guarding reduced the risk of sperm competition. Although male-male competi- tion appears to be the dominant factor in pair-formation, the ability of females to extend their recep- tivity in the absence of males, will have an impact on the operational sex ratio, and on the extent of male-male and sperm competition.

Reproductive Behavior of Ground Weta (Orthoptera: Anostostomatidae): Drumming Behavior, Nuptial Feeding, Post-copulatory Guarding and Maternal Care

Compared to other ensiferan Orthoptera such as true crickets (Gryllidae) and katydids (Tettigoniidae) relatively little is known about the reproductive behavior of Anostostomatidae (formerly Stenopelmatidae), the king crickets, weta and allies. Moreover, although the New Zealand species (the weta) are best known, there is little knowledge of the biology of ground weta (Hemiandrus species), a variable genus especially with regard to ovipositor length. This paper presents observations of mating and post-mating behavior of several Hemiandrus species with short ovipositors. Sexually active males and females drum their abdomens on the substrate, apparently as local signals for mate attraction (pheromones may be involved in long distance communication). After mating there is both maternal and paternal investment. Females provide care to eggs and young larvae and males provide a spermatophylax to the female, a mating meal that, in other ensiferan Orthoptera can be an important source of nutrition. In contrast to other ensiferans, however, the spermatophylax of Hemiandrus species with short ovipositors is deposited on the female's abdomen, a separate location from the sperm ampulla. The spermatophylax is deposited while the male is attached to the female's underside, apparently to her modified 6th abdominal sternite. Also, in contrast to related taxa, males remain with their mates while the mating meal is eaten. These observations indicate that ground weta are excellent systems for examining behavioral and ecological questions about the evolution of complex signals, as well as the evolution of maternal and paternal investment.

Observation on the Mating Behaviour of the Helmet Crab Telmessus cheiragonus (Brachyura: Cheiragonidae)

The mating behaviour of the helmet crab, Telmessus cheiragonus, was observed in the laboratory to obtain information of its fishery management and seed production. Females always moulted before copulation and all moulting females copulated with their mates, while males performed precopulatory guarding before their mates moulted. The average duration of precopulatory guarding was 11.8±5.0 SD days. Sex ratios in experimental tanks did not influence the first guarding duration of male but diminished the female's guarded duration under female-biased treatment. Competition among males for females was observed; larger males appeared to have a competitive advantage. Males started copulation in 41.2±10.9 SD min after females moulted and the copulation lasted for 110.6±6.6 SD min. Postcopulatory guarding duration was 4.0±6.6 SD h. Small males tended not to guard and to copulate with females larger than themselves. Common features and differences in mating behaviour between T. cheiragonus and Erimacrus isenbeckii is discussed.

Experimental analysis of the effect of genital morphology on insemination success in the ground beetle Carabus insulicola (Coleoptera Carabidae)

The hypothesis that the elaborated genitalia of male insects serve to improve insemination success were tested using the ground beetle Carabus insulicola. To enhance variation in genital size, the genital hooks of experimental males were cut, and these males were then mated with virgin females. Logistic regression showed that the length of the male genital hook affected insemination success. Males with a shorter genital hook tended not to deposit spermatophores at the proper site, and failed to transfer sperm into the spermatheca. Therefore, the male genital hook serves to increase insemination success by depositing a spermatophore at the site where sperm are likely to be transferred. The duration of copulation and post-copulatory guarding may also be explained by these determinants. Stepwise regressions indicated that the occurrence of ejaculation, and the location of the spermatophore determined the duration of copulation and post-copulatory guarding, respectively.

Mating strategy of spider mite, Tetranychus urticae(Acari: Tetranychidae) males: Postcopulatory guarding to assure paternity.

Precopulatory guarding behavior in males of Tetranychus urticae occurs because only the first mating is effective for females. Sufficient copulation duration to fertilize females in the laboratory is shorter than it is in nature. This finding leads to the hypothesis that the copulation duration of T. urticae is prolonged by postcopulatory guarding which prevents the female from remating with other males. To test this hypothesis, we manipulated the interval between the first and second copulations of a female. A significant positive correlation was detected between the mating interval and the proportion of daughters fathered by the first male of each brood. Males using postcopulatory guarding are successful when other males disturb the mating pair to take over from the mating male. These results demonstrate that males gain from prolonged copulation that prevents a female from remating until their sperm precedence is assured. Thus, males of T. urticae increase their paternity not only by precopulatory guarding but also by the postcopulatory guarding.

Population density influences male–male competition in guppies

This study tested the general prediction that population density affects male–male competition, female mate choice and the opportunity for sexual selection. By manipulating the density of guppies, Poecilia reticulata, while keeping the sex ratio constant, I found that male mating tactics were phenotypically plastic with respect to density. As density increased, males decreased their courtship displays. Male–male competition and mate searching were highest at intermediate densities. Population density had no significant effect on the total number of copulations, copulatory tactics or the percentage of postcopulatory guarding. Female preference for males with a higher percentage of orange coloration was similar at all density levels. The ‘opportunity for sexual selection’, which estimates the upper limit to which a selected trait can shift if directional selection is operating and was calculated as the variance in number of copulations per male divided by the square of the mean number of copulations, was negatively associated with population density. This may be due to the decrease in male–male competition at high density rather than female preference which was similar across density treatments.

Operational sex ratio influences female preference and male–male competition in guppies

Manipulation of the operational sex ratio (OSR) in guppies, Poecilia reticulata, causes changes in male–male competition and female mate choice. In this study OSR is defined as the number of sexually active males divided by the total number of sexually active adults of both sexes. The rate of male courtship displays decreased, and interference behaviours between males increased, at male-biased OSRs. The OSR influenced both copulatory tactics and postcopulatory guarding. All copulations followed sigmoid displays, except at an OSR of five males to one female where 60% of copulations occurred during sneak attempts. Compared with copulations that followed sigmoid displays, successful sneak copulations were followed by a shorter period of postcopulatory mate guarding and a shorter refractory period before males resumed courtship activities. Females preferred males with more orange colour whenever they had a choice, and the preference for orange colour was stronger with more male-biased OSRs. The OSR thus influences the presence, absence or relative importance of both female mate choice and male–male competition which, in turn, should affect the evolution of secondary sexual traits.

Mating and role of seminal receptacles in the reproductive biology of the spider crab Maja squinado (Decapoda, Majidae)

The reproductive biology of the spider crab Maja squinado was analyzed based on monthly samples from an 18-month study carried out in Galicia (NW Spain) and laboratory experiments holding primiparous and multiparous females in captivity with and without males. The seminal receptacles of adult females were analyzed and their relationship with the presence and developmental stage of the eggs and the gonad maturity stage was determined. Gonad maturation in primiparous females began one or two months after the pubertal moult. Females having gonads in an advanced stage of development made their appearance in December and the first spawning took place in mid-winter or early spring. The percentage of ovigerous females from March to September was ∼75%. As the incubation period progressed, the ovaries became mature again in order to carry out the next spawning. Under experimental conditions the breeding cycle started earlier in multiparous females, during their second yearly cycle, than in primiparous ones. After mating, female spider crabs store sperm in seminal receptacles and this sperm is used in the fertilization of eggs immediately prior to spawning. The analyses of seminal receptacles consisted of the estimation of fullness and the number of differentiated sperm masses. The number of masses ranged between 0 and 6 in field samples (median for females with stored sperm=1) and was positively correlated with fullness. Differences in colour and volume of individual masses showed that, at least in some cases, females carried out successive matings with long intervals in between. This storage mechanism allowed females to fertilize successive broods without remating (as was also shown under experimental conditions). Juvenile females from shallow waters did not have developed seminal receptacles which indicated that mating was not possible until the onset of maturity. Postpubertal females in shallow waters (August to October), including animals participating in aggregations, always showed empty receptacles. The seasonality of receptacle fullness showed that mating involved hard-shelled females and occurred in deep water during the autumn migration from juvenile habitats or in the wintering habitats, during the last stages of gonad maturation (November to February). After fertilization ovigerous females continued to store sperm, but the volume was lower than in non-ovigerous females. Mating may occur in ovigerous females, particularly in the final period of incubation, because in females with broods almost ready to hatch, both new and older sperm masses were seen in the receptacles (distinguished by colour and size). The fullness of the receptacles decreased both in ovigerous and non-ovigerous females in the final phase of the annual breeding cycle (August–October), however, some sperm was still available. In the laboratory, mating was observed, and no courtship nor postcopulatory guarding was recorded. The analysis of receptacles from laboratory experiments indicated that primiparous and multiparous females showed differences in the seasonality of mating in the first phase of the breeding cycle (September–January), related to differences in the timing of gonad maturation and hatching. Mating occurred in the final stages of gonad maturation, a short time before hatching, and matings were detected in ovigerous females. Multiple matings were also evident, to a greater extent than in the field, probably due to the higher availability of males. Females underwent over four successive spawnings in the laboratory without having to recopulate, and the incubation lasted on the average from 40 to 58 days (∼18 and 16°C respectively) and the mean duration between hatching and the next spawning was 3.4 days. It is estimated that most females carry out three successive spawnings during the annual cycle.

THE ROLE OF TERRITORIALITY IN THE MATING SYSTEM OF THE SPRINGBOK ANTIDORCAS MARSUPIALIS

SUMMARY The role of territoriality was examined in relation to the breeding system of the springbok, Antidorcas marsupialis, in the southern Kalahari. Males defended territories in areas where the polygyny potential was highest. During the rut females appeared to be attracted primarily to the resources on a territory and not to the rams themselves. Only males who successfully defended territories were observed to breed with females, though females were often mated more than once and sometimes by more than one male. Male springbok showed no pre- or post-copulatory guarding behaviour, whilst oestrous females did not choose to join larger groups in order to avoid harassment by other males. The results of this study are compared to those from lek-breeding ungulates.

The relationship between mating system and penis morphology in ischnuran damselflies (Odonata: Coenagrionidae)

Zygopterans belonging to the genusIschnuraare unusual amongst damselflies because of the variety of mate guarding techniques employed by males of different species. The lack of post-copulatory guarding combined with lengthy copulations in one group of ischnuran species suggest that these males guard femalesin copula. An examination of the accessory penes of species in this group indicates that all but one species have considerable microspination on the distal end (the flagella) of their penes that can function in sperm displacement. The flagella of these species are long and thin compared to those of other ischnurans. This is likely an adaptation to gain access to the spermatheca of the female. Two species tandem guard their mates during ovipositing. These species are the only ischnurans missing a stout pair of basal spines on the penultimate segments of their penes. They have considerable microspination over much of their penes but their flagella are of only moderate length and stout. Ischnurans that do not mate guard have short, stout flagella and most species examined from this group (5 of 7) have little microspination on their flagella tips. It is proposed that females of these species mate only once and therefore their males do not displace sperm.

The relationship between mating system and penis morphology in ischnuran damselflies (Odonata: Coenagrionidae)

Zygopterans belonging to the genus Ischnura are unusual amongst damselflies because of the variety of mate guarding techniques employed by males of different species. The lack of post-copulatory guarding combined with lengthy copulations in one group of ischnuran species suggest that these males guard females in copula . An examination of the accessory penes of species in this group indicates that all but one species have considerable microspination on the distal end (the flagella) of their penes that can function in sperm displacement. The flagella of these species are long and thin compared to those of other ischnurans. This is likely an adaptation to gain access to the spermatheca of the female. Two species tandem guard their mates during ovipositing. These species are the only ischnurans missing a stout pair of basal spines on the penultimate segments of their penes. They have considerable microspination over much of their penes but their flagella are of only moderate length and stout. Ischnurans that do not mate guard have short, stout flagella and most species examined from this group (5 of 7) have little microspination on their flagella tips. It is proposed that females of these species mate only once and therefore their males do not displace sperm.

Operational Sex Ratios and Mating Conflict between the Sexes in the Water Strider Gerris lacustris

This is the first study to highlight the importance of individual operational sex ratio (OSR) experience in altering mating behavior and intersexual conflict over mating in insects. Reproductively active Gerris lacustris were held under highly male- or female-biased sex ratios and then tested in various treatment combinations with either male- or female-biased sex ratios. With our manipulations we disentangled the effect of experienced and ambient (mating environment) OSR, separately for females and males, which allowed the assessment of the differing contributions of male persistence and female reluctance in mating. Only male OSR experience affected the duration of mating: males from male-biased environments increased the length of copulation and postcopulatory guarding and the proportion of guarding of total duration of mating. Female-biased experience of both sexes resulted in short matings with practically no guarding, and males dismounted before females started struggling. Males from male-biased and ...

On the post-copulatory guarding behaviour of male field crickets

On the post-copulatory guarding behaviour of male field crickets

On the biology of the damselfly Nososticta kalumburu Watson & Theischinger (Zygoptera: Protoneuridae)

The habitat and the territorial and reproductive behaviours of a recently named Australian protoneurid damselfly, Nososticta kulumburu Watson & Theischinger are described. Nososticta kalumburu breeds in shallow, narrow (<2 m wide) fast-flowing permanent streams in the Kimberley region of Western Australia. The presence of suitable perches (protruding rocks or overhanging vegetation) seems to be important in determining its distribution. It is a sexually dimorphic species; males have prominent dark brown spots on the wings and a blue pruinescence, which the females lack. Males are strongly territorial. Territories (radius around I m) are small in both high and low density populations and are defended vigorously against conspecific males. Male courtship behaviour towards potential mates involves a vigorous hovering flight in front of, and by the side of, the female, during which the prominent dark brown spots on all four wings are dispalyed. Mean length of copulation is 15.4 min. Two stages of copulation were recognized. It is thought that the first stage which occupies most time (94.7%) is concerned with removing sperm from previous matings in the usual zygopteran manner. Oviposition begins in tandem in the stems of aquatic macrophytes or the roots of terrestrial plants that hang into thc water. Males exhibit plasticity in post-copulatory guarding bchaviour: in pairs undisturbed during the early stages of oviposition, the male may release the female before the current bout of egg-laying has been completed and attempt to regain a territory. The penis is unusual in having a heavily armoured shaft and two pairs of cornua; it is probably used in sperm removal as well as intromission.

Post-copulatory guarding, female choice and the levels of gregarine infections in the field cricket, Gryllus bimaculatus

A recent model in sexual selection has proposed a role for parasites in maintaining heritable fitness variation. Females are envisaged as benefitting from preferentially mating with males that show resistance to infection. The post-copulatory guarding behaviour characteristic of many species of field cricket, has been envisaged as a means by which females assess male health and vigour. This hypothesis was tested in a field cricket, G. bimaculatus, which harbours a protozoan gut parasite. In enclosed arena trials, no direct correlations between female behaviours and levels of infection in males were found. However, there were significant correlations between the intensity of male guarding and the number of parasites found in the gut; infected males guarded more intensely in order to maintain contact with the female. In a second experiment simulating open field conditions, females left heavily parasitized males sooner than mildly or uninfected individuals. These data are discussed in relation to female choice for male health and vigour.

The influence of sexual selection and predation on the mating and postcopulatory guarding behavior of stone crabs (Xanthidae, Menippe)

Postcopulatory mate guarding in crustaceans traditionally has been viewed as a behavioral mechanism that prevents predation on the soft post-molt female. This study tests the effects of sexual selection and predation on the postcopulatory guarding durations of male stone crabs, Menippe mercenaria, M. adina, and their hybrid. Male stone crabs were held with a pre-molt female, and either another adult male stone crab, an intermolt female, or a male blue crab, which corresponded to intermale competition, control, and predation treatments, respectively. The mating behavior of the heterosexual pair was recorded with a time lapse video system and the durations of copulation and postcopulatory guarding were measured. Males guarded longer in the intermale competition treatment than either the control or predation treatments. In the competition treatment, agonistic encounters occurred between the males at the den containing the female and several mate takeovers occurred. Females survived the predation treatment in trials in which the guarding durations were the longest, whereas females were eaten by the blue crab in trials with the shortest guarding durations. Sexual selection appears to be important in maintaining postcopulatory mate guarding in stone crabs.