Does Female Personality Determine Mate Choice Through Sexual Cannibalism?

Animal personalities (e.g. consistent across‐context behavioural differences between individuals) can lead to differences in mate choice. However, evidence for this link remains limited. Pre‐mating sexual cannibalism can be a behavioural syndrome (i.e. a suboptimal personality) in which adaptive female aggression towards heterospecific prey spills over on non‐adaptive aggression towards courting males, independently of the female mating or feeding status (i.e. the ‘aggressive spillover hypothesis’, ASH). On the other hand, sexual cannibalism can also be a form of mate choice by which females selectively kill or mate with males depending on the male phenotype. We introduce the hypothesis that the most aggressive females in the population will not only attack males more frequently, but will be less likely to impose sexual selection on males through sexual cannibalism. Assuming that in a field common garden experiment in which females were fed ad libitum the rate of weight gain by a female may reflect her voracity or aggressiveness, we show that in the cannibalistic burrowing wolf spider Lycosa hispanica (formerly L. tarantula), voracity towards heterospecific prey predicts a female's tendency towards sexual cannibalism. Unmated females with higher weight gains were more cannibalistic and attacked males regardless of the male phenotype. On the other hand, females that were less voracious tended to be less cannibalistic, and when they did kill a male, they were selective, killing males in poorer condition and mating with those in better condition. Our results demonstrate that females with different phenotypes (growth rates) differently imposed selection on male condition, tentatively supporting the hypothesis that female aggression levels can spill over on sexual selection through sexual cannibalism.     

The nutritional contribution of males affects the feeding behavior and spatial distribution of females in a bruchid beetle,<Emphasis Type="Italic"> Bruchidius dorsalis</Emphasis>

The relationship between the quality/quantity of male investment and the feeding behavior of females was investigated in a bruchid weevil, Bruchidius dorsalis (Fahraeus), whose males donate nutrition via seminal fluid to females. Experiments on the effect of feeding regimes of both sexes on the mating frequency of females showed that females mated at a higher frequency if given low-quality food or poor male investment. On the other hand, the experiment that examined the effect of male investment quality on female feeding behavior showed that females receiving the high-quality investment exhibited feeding behavior less often. These results suggest that male investment and feeding behavior play the same role for B. dorsalis females. These experiments also showed that there are sex-related asymmetries in mating and feeding behaviors: females mated more often but males fed more often. Moreover, a field census suggested that only males visited non-host flowers to feed on the pollen and nectar during the non-flowering period of the host plants; females always stayed on the host plants irrespective of the flowering phenology. These results suggest that in B. dorsalis courtship role reversal and sex-specific feeding modes are fairly fixed and obligatory, and that male investment, derived from sexual selection, could affect the feeding behavior and spatial distribution of both sexes, which may have far-reaching impact in various ecological contexts.     

Male mate choice in the gynogenetic–sexual complex of crucian carp,<Emphasis Type="Italic"> Carassius auratus</Emphasis>

The asexual all-female Japanese crucian carp, Carassius auratus langsdorfii (Teleostei: Cypriniformes), reproduces gynogenetically, relying on the sperm of males of the sexual "host," C. auratus subspp. Theoretically, frequency-dependent mating preference of males to conspecific females can lead to the coexistence of asexual and sexual fish, if all else is equal. Our specific questions are whether males prefer conspecific females over asexual females and whether individuals show dominance hierarchies that potentially cause frequency-dependent mating preference. In an individual choice experiment, a tank was partitioned into three compartments with the middle one for a single male and the two outer ones for a sexual and an asexual female. The males of C. auratus bürgeri demonstrated a significant preference for ovulated conspecific females over ovulated asexual females. In contrast, in a group mating experiment, a single experimental tank included two males, a sexual female, and an asexual female together, and males chased and mated with both asexual and sexual females equally. Male mate preference was weak in group mating, which is typical in natural populations. Males and females of crucian carp showed no apparent agonistic behavior to each other in the group mating experiment. This is different from other gynogenetic complexes with the dominance hierarchy of males showing strong frequency-dependent mating preference (e.g., Poeciliopsis). We conclude that male mate preference is unlikely to be a strong frequency-dependent force maintaining the coexistence of asexual–sexual complexes of Japanese crucian carp. Received in revised form: 5 February 2001 Electronic Publication     

Female choice for heterozygous mates changes along successive matings in a lizard

Female mate choice and female multiple mating are major focuses of studies on sexual selection. In a multiple mating context, the benefits of mate choice can change along successive matings, and female choice would be expected to change accordingly. We investigated sequential female mate choice in the moderately polyandrous common lizard (Zootoca vivipara, synonym Lacerta vivipara). Along successive mating opportunities, we found that females were relatively unselective for the first mate, but accepted males of higher heterozygosity for subsequent mating, consistent with the trade-up choice hypothesis. We discuss the evidence of trade-up mate choice in squamates and generally trade-up for mate heterozygosity in order to motivate new studies to fill gaps on these questions.     

Male pioneering as a mating strategy: the case of the beetle Maladera matrida

1. The phenomenon of male pioneering, whereby males are active (daily) before females, is compared with protandry, a phenomenon whereby males are sexually matured before females. The effects of natural selection and sexual selection on both phenomena are discussed. 2. In Maladera matrida Argaman (Coleoptera: Scarabaeidae), males emerged from the soil a few minutes before females, every evening, to feed and mate. 3. Aggregations of males and females are formed at sites of plant damage where males initiated feeding. 4. All copulations were initiated at the beginning of the activity period so males that emerge earlier may increase their probability of finding a mate. 5. Females mate only once in an evening. 6. Males that emerge later may not find receptive females with which to mate. 7. The aggregation of beetles per se did not contribute to the individual mating success because it occurred during and after the copulating had begun. 8. Male pioneering may evolve through sexual selection by means of male–male competition in time to achieve receptive females.     

Sexual Strategies of a North American ‘Tarantula’ (Araneae: Theraphosidae)

Despite their general notoriety and popularity as pets, little is known of the behavioural ecology of ‘tarantulas’ or theraphosid spiders. We studied a theraphosid of the Arizona deserts, Aphonopelma sp., to determine behavioural events crucial to successful courtship and mating. Males search for spatially scattered females and, at short range, may detect females by substrate-borne cues. When two males are present with a single female, no direct competition such as aggression is observed. Both males may mate with a single female in rapid succession, with no evidence of post-copulatory mate guarding. Despite the potential for sexual cannibalism, courtship and mating behaviour patterns exhibit few aggressive elements and males nearly always survive sexual encounters with females. The mating system of this Aphonopelma species may best be described as a type of scramble-competition polygyny, in which the ability of males to locate receptive females is an important determinant of mating success in males. Multiple mating by females renders predictions concerning fertilization success uncertain, due to the possibility of sperm competition and ‘cryptic’ female mate choice.     

Mating Tactics in Response to Costs Incurred by Mating with Multiple Males in Wild Female Japanese Macaques

We investigated the costs of mating with multiple males in terms of feeding time, traveling distances, sexual proceptivity, and male aggression, for wild female (Macaca fuscata yakui) on Yakushima Island, Japan. We analyzed all-day focal sampling data from 7 females during the mating season (Sept.-Nov. 1996). On days when estrous females copulated with multiple males, they decreased their feeding time to half that of anestrous days, traveled longer distances, showed more proceptive sexual behaviors and received more aggression from subordinate males than on days when they copulated with only the 1st-ranking male. On days when females copulated with only the 1st-ranking male, they showed no difference in feeding time with that of anestrous days, and expended less effort than the above mating pattern because of short traveling distances, diminished sexual proceptivity and a lower frequency of aggression received. The results suggest that the costs of estrous vary according to female sexual proceptivity and the number and social status of mating partners. Female Japanese macaques exhibit a mixed mating strategy over prolonged estrous periods, which may provide females with opportunities to maximize the benefits of copulating with multiple males and to minimize the costs of estrus by mating with only the 1st-ranking male. During an estrous cycle, females may be adjusting efforts for reproduction and survival; i.e., mating vs. feeding.     

Seasonal aspects of sexual cannibalism in the praying mantis (<Emphasis Type="Italic">Mantis religiosa</Emphasis>)

According to the adaptive foraging hypothesis of sexual cannibalism, females face a trade-off between mating and consuming a courting male. Because male and prey availability can change seasonally, sexual cannibalism may change with season. However, we are not aware of any work examining how sexual cannibalism in insects relates to the time of season. Here, we examined the seasonal pattern of sexual cannibalism and reproductive behaviour in the sexually cannibalistic praying mantis (Mantis religiosa). We repeatedly collected the last instars of praying mantises from the field and brought them up under natural weather and photoperiod, but standardised feeding and socioecological conditions. After the females reached sexual maturity, we allowed all of the females to mate during two mating trials. In comparison to female praying mantises maturing later in the season, early-maturing females were larger but of poorer body condition on the day of a mating trial (20 days after the adult moult). During the first round of mating trials, early-maturing virgin females cannibalised males more frequently than their late-maturing counterparts. In contrast, late-maturing females that mated in the first round of mating trials were more likely than early-maturing, nonvirgin females to be cannibalistic in the second round of mating trials. The latency time until copulation was correlated with a risk of sexual cannibalism and was longer in early-maturing females. Our study suggests that the date of the last (adult) moult plays an important role in the occurrence of sexual cannibalism.     

Effect of delayed mating and prolonged engorgement on the reproductive fitness of female Amblyomma limbatum (Acari: Ixodidae) in marginal population areas

Reptile ticks mate while females are attached to their host. Following mating, females engorge, detach and then lay their eggs. This study examines whether the time that females of the reptile tick Amblyomma limbatum spend on hosts prior to mating and the time they take to engorge on hosts after mating influence their reproductive fitness, as measured by the number of viable eggs they produce. When compared with females that experienced no temperature-induced delay in mating, females attached for an initial period to hosts with body temperatures too low to induce mating had no decline in their reproductive fitness, once provided with suitable temperatures for mating. However, on hosts with suitable body temperatures for mating, female ticks that took longer to mate, took longer to engorge and had reduced reproductive fitness. In addition, females that spent more than 20 days feeding on hosts after mating had reduced reproductive fitness, irrespective of the time they spent on hosts prior to mating compared with females with shorter feeding periods. Thus, the time that A. limbatum females spent on hosts prior to mating and/or after mating has a significant bearing on the number viable progeny produced. The ecological implications of these results are discussed in relation to females colonizing marginal population areas at the edge of their distributional range.     

Removal of Surface Glycoproteins and Transfer among <Emphasis Type="Italic">Brachionus</Emphasis> species

Glycoproteins on the body surface of females of the rotifer Brachionus plicatilis are a key signal in their mate recognition system. When B. plicatilis Russian strain females were exposed to 50 mM EDTA or EGTA, several surface glycoproteins were removed. Females exposed to EDTA died, but remained intact and were used in mating bioassays with conspecifics males. Live control females elicited a male mating response in 21% of encounters, freeze-killed control females elicited responses in 23%, but EDTA extracted females elicited a mating response in only 5% of encounters. At least some of the EDTA-extractable proteins on the surface of females appear to be critical to male mate recognition. EDTA treated females could be exposed to proteins extracted from other females and some proteins re-attached to their body surface, restoring their attractiveness to males. SDS-PAGE of these proteins revealed 15–17 prominent bands, most ranging in molecular mass from 66 to 12 kD. The EDTA-extractable proteins were separated using ion exchange chromatography and each fraction was tested for its ability to restore female attractiveness. When proteins in fraction 22 were bound to females, they restored 80% of the females’ ability to elicit male mating responses. Exposing EDTA treated females to bovine serum albumin or casein had no effect on their attractiveness to males. EDTA treated females from different Brachionus clades and species were exposed to proteins from fraction 22. Female attractiveness could be restored in most clades of B. plicatilis, but no transfer of mating attractiveness was observed to B. rotundiformis or B. ibericus females. Conspecific males treated with EDTA and exposed to proteins in fraction 22 could not be feminized and made attractive to other males. A sexual dimorphism in surface proteins therefore exists between B. plicatilis females and males. Successful transfer of glycoproteins critical in mate recognition is dependent on signal glycoprotein structure and the structure of the other proteins present on the surface of females.     

Divergent host plant adaptation drives the evolution of sexual isolation in the grasshopper Hesperotettix viridis (Orthoptera: Acrididae) in the absence of reinforcement

Early stages of lineage divergence in insect herbivores are often related to shifts in host plant use and divergence in mating capabilities, which may lead to sexual isolation of populations of herbivorous insects. We examined host preferences, degree of differentiation in mate choice, and divergence in cuticular morphology using near‐infrared spectroscopy in the grasshopper Hesperotettix viridis aiming to understand lineage divergence. In Kansas (USA), H. viridis is an oligophagous species feeding on Gutierrezia and Solidago host species. To identify incipient mechanisms of lineage divergence and isolation, we compared host choice, mate choice, and phenotypic divergence among natural grasshopper populations in zones of contact with populations encountering only one of the host species. A significant host‐based preference from the two host groups was detected in host‐paired feeding preference studies. No‐choice mate selection experiments revealed a preference for individuals collected from the same host species independent of geographic location, and little mating was observed between individuals collected from different host species. Female mate choice tests between males from the two host species resulted in 100% fidelity with respect to host use. Significant differentiation in colour and cuticular composition of individuals from different host plants was observed, which correlated positively with host choice and mate choice. No evidence for reinforcement in the zone of contact was detected, suggesting that divergent selection for host plant use promotes sexual isolation in this species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 866–878.     

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.

     

Costs of Mate Guarding and Opportunistic Mating Among Wild Male Japanese Macaques

A trade-off relationship between mating and feeding effort is important when considering reproductive strategies of long-lived species. I compared the influence of male sexual activities, female mate-choice behaviors and the daily activity budget on male mating success among males in a group of wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. The 1st-ranking male, which had immigrated into the troop at this rank, more frequently approached peri-ovulatory females, spent more time grooming peri-ovulatory females and in mounting series and spent less time feeding than subordinate males did. The 1st-ranking male attained the highest mating success as a result of his high expenditure of time and energy in sexual behaviors directed toward peri-ovulatory females. Mating success of subordinate males did not relate to the amount of sexual effort, but instead to the frequency of female approaches, female rush toward males and the number of peri-ovulatory females within the group. The pattern of intermale competition shifted from nearly contest competition to scramble competition as the number of peri-ovulatory females in the group increased. Feeding time of subordinate males did not vary between the days when they copulated and the days when they did not. The findings demonstrate that mate guarding in the 1st-ranking male is a high-cost mating tactic, while opportunistic mating in subordinate males is a low-cost mating tactic. The differences in male mating tactics are probably related to male life history and to the formation of groups with a high socionomic sex ratio.     

Protandry in the parasitoidCardiochiles nigriceps,as related to its mating system

A laboratory study was conducted of the emergence times and mating success ofCardiochiles nigriceps Viereck (Hymenoptera: Braconidae), a larval parasitoid of the tobacco budworm,Heliothis virescens (F.) (Lepidoptera: Noctuidae), and in view of this information, the parasitoid's mating system was explored. Observations on laboratory populations ofC. nigriceps confirmed the occurrence of two types of protandry, i.e. seasonal and diurnal; males emerged 2 days before females in a generation, and emerged about 1 hr before females on a given day. An experiment on mating success showed that newly emerged females are not receptive to males that emerged 1 hr earlier, but that these males and females often mate successfully after 1 more hr. The experiment also showed that 1- to 5-day-old males are more successful than 1-hr-old males in mating with 0- to 1-hr-old females. Thus, it is argued that males emerging on a given day have a disadvantage in competition for mates with males that emerged days earlier, and that this disadvantage may serve as a selection pressure toward diurnal protandry. A monogamous mating system for females ofC. nigriceps is suggested because sexual selection would be expected to be strong in species exhibiting both seasonal and diurnal protandry. A possibility of a sibling mating system inC. nigriceps is questioned partly because newly emerged females are unreceptive to males that emerged 1 hr earlier and partly because this parasitoid is solitary in what is considered highly dispersed hosts in the field.     

Male-biased sex ratios,female promiscuity,and copulatory mate guarding in an aggregating tropical bug,Dysdercus bimaculatus

The ecological and social bases of the mating system of the seed-feeding bug, Dysdercus bimaculatus(Hemiptera: Pyrrhocoridae), were studied in the lab and in aggregations at the host tree, Sterculia apetala(Malvales: Malvaceae), in Panama. On theoretical grounds, two factors are predicted to be of importance in determining the evolution of male mating tactics in Ms species: the operational sex ratio and the probability that undefended females will mate with other males, subjecting the gametes of deserters to sperm competition. Results of a study of a related species suggested that sperm displacement is probably substantial. Adult sex ratios at numerous sites were significantly male biased, and females whose mates were removed remated before oviposition (i. e., sperm utilization). These results predict that a mate defense tactic is likely to be superior to a nondefense tactic. The biological significance of the parameters is supported by observations that captive pairs often remained in copulafor several days, until just before oviposition. However, substantial variation in copulation duration was also observed, and possible causes of this variation are considered. Causes of male biased adult sex ratios were investigated by monitoring demographic changes within a single aggregation over 2 months. Both female juvenile and adult mortality rates were greater than male. In addition, dissections of reproductive adults showed that the flight muscles of females, but not males, had histolyzed, so that female reproduction is physiologically limited to a single site. Greater rates of immigration among both mature and young males suggests that an excess of males may also be found in the populations of bugs that subsequently colonize other host plants, so that female scarcity is typical of aggregations in all stages of development. The evolution of sex-limtied flight muscle histolysis may be explained by greater patchiness of females than males as mating resources, plus a lower energetic benefit/cost ratio of histolysis for males.     

First evidences of sexual selection by mate choice in marine zooplankton

Sexual selection is potentially important in marine zooplankton, presumably the most abundant metazoans on earth, but it has never been documented. We examine the conditions for sexual selection through mate choice and describe mating preferences in relation to size in a marine zooplankter, the pelagic copepod Acartia tonsa. Males produce spermatophores at a rate (~1 day⁻¹) much lower than known female encounter rates for most of the year and the decision to mate a particular female thus implies lost future opportunities. Female egg production increases with female size, and males mating larger females therefore sire more offspring per mating event. Similarly, females encounter males more frequently than they need to mate. Large males produce larger spermatophores than small males and the offspring production of female increases with the size of the spermatophore she receives. Additionally, large spermatophores allow females to fertilize eggs for a longer period. Thus, mating with large males reduces the female’s need for frequent matings and she may sire sons that produce more offspring because size is heritable in copepods. Finally, we show that both males and females mate preferentially with large partners. This is the first demonstration of sexual selection by mate choice in a planktonic organism.     

Interspecific interactions and learning variability jointly drive geographic differences in mate preferences

Co‐occurrence of closely related species can cause behavioral interference in mating and increase hybridization risk. Theoretically, this could lead to the evolution of more species‐specific mate preferences and sexual signaling traits. Alternatively, females can learn to reject heterospecific males, to avoid male sexual interference from closely related species. Such learned mate discrimination could also affect conspecific mate preferences if females generalize from between species differences to prefer more species‐specific mating signals. Female damselflies of the banded demoiselle (Calopteryx splendens) learn to reject heterospecific males of the beautiful demoiselle (C. virgo) through direct premating interactions. These two species co‐occur in a geographic mosaic of sympatric and microallopatric populations. Whereas C. virgo males have fully melanized wings, male C. splendens wings are partly melanized. We show that C. splendens females in sympatry with C. virgo prefer smaller male wing patches in conspecific males after learning to reject heterospecific males. In contrast, allopatric C. splendens females with experimentally induced experience with C. virgo males did not discriminate against larger male wing patches. Wing patch size might indicate conspecific male quality in allopatry. Co‐occurrence with C. virgo therefore causes females to prefer conspecific male traits that are more species specific, contributing to population divergence and geographic variation in female mate preferences.     

Opportunities for mate choice in the fission‐performing ant Cataglyphis cursor

1. Sexual selection has been little studied in social insects. Nonetheless, because mating is generally for life, opportunities for selecting among mating partners should be exploited. 2. In some ants, males aggregate at nest entrances to mate with emerging gynes. Both males and females thus have access to multiple mates over a relatively protracted period, giving rise to opportunities for mate choice and multiple mating. 3. We provide data from field observations of the male mating biology of the ant, Cataglyphis cursor Fonscolombe. In this species, females mate with, on average, six males each at the nest entrance and found colonies with the help of workers. 4. Males were present at the field site for approximately 1 month in spring, with up to 40 males at a single nest entrance for, on average, 4.7 days. Individual males were observed to survive up to 3 days, and mate up to eight times. 5. Thus both males and females of this species have the ability to mate multiply and have a window permitting mate choice to occur. Workers actively attacked males and may take part in the mate choice process, making C. cursor an interesting model to study questions relating to sexual selection and male mating strategies.     

Size-biased Mating in Both Sexes of the Black-horned Tree Cricket, <Emphasis Type="Italic">Oecanthus nigricornis</Emphasis> Walker (Orthoptera: Gryllidae: Oecanthinae)

Previous studies on tree crickets have demonstrated female choice of males based on size and courtship feeding but less is known about sexual selection under conditions of direct mating competition. I studied courtship, aggression and mating of the black-horned tree cricket Oecanthus nigricornis (Walker) to test size-related sexual selection under conditions of direct sexual competition. Results show that larger individuals of both sexes mated more frequently than their smaller counterparts, and this was due to the ability of large individuals to out compete rivals. Large males achieved the advantage by aggressively reducing courtship by small males, whereas large females responded to male courtship more quickly but with little aggression. Although there was no evidence here for mate choice, there were advantages for having larger mates; fecundity increased with female size and spermatophores (which females consume after mating) increased with male size. Size of the specialized metanotal courtship gift, however, was not related to male size.     

HOST-PLANT-INDUCED ASSORTATIVE MATING IN ENCHENOPA TREEHOPPERS

The hypothesis tested here is whether extrinsic host-plant-induced life-history timing and mating biology promote assortative mating along host-plant lines. In the arboreal, univoltine Enchenopa treehopper system, host plants mediate the timing and synchronization of egg hatch. The result is a uniform age structure with a restricted mating window during which females mate once. Enchenopa on host plants that differ in phenology have asynchronous life histories and mating windows, suggesting that temporal differences may promote assortative mating. To test this hypothesis, egg hatch of Enchenopa from the same host-plant species was manipulated to produce continuous adult age-classes. Under experimental conditions with no spatial barriers, mating occurred between individuals similar in age. The mechanism promoting this assortative mating is differential mortality in males and females, such that few males are still alive when females in successive age-classes mate. Such host-plant-induced assortative mating is viewed as an effective mechanism to protect the integrity of gene pools from migrants, permitting selection for host-plant-adapted genotypes and speciation.