A SEX DIFFERENCE IN THE PROPENSITY TO ENTER DIRECT/DIAPAUSE DEVELOPMENT: A RESULT OF SELECTION FOR PROTANDRY

In monandrous mating systems with discrete nonoverlapping generations males should maximize the expected number of matings by starting to emerge before females. This is known as protandry. Moreover, Evolutionarily Stable Strategies (ESS) models show that the male emergence curve should be abruptly truncated before female emergence has ceased. In temperate areas where many insects have partial second generations, we accordingly predict that males should enter diapause development at an earlier date than should females, as a result of late-emerging males being penalized in terms of fewer mating opportunities. The decision to diapause or to develop directly is usually mediated by response to environmental stimuli of which day length is the most important. Hence we predict that the mechanism by which males enter diapause at an earlier date than females will be that of the male reaction norm for diapause development being shifted towards longer day lengths when compared to that of females. As a result of the greater tendency of males to enter diapause development, partial second generations that develop directly should be female biased. As a corollary, first generations should be male biased because some males of the first generation are from the previous year. The prediction that males should enter diapause development earlier in the season, i.e., at longer day lengths, as compared to females was corroborated by rearing Pieris napi under a variety of critical day length regimes producing mixed broods of directly developing and diapausing individuals, and by outdoor rearings of cohorts of larvae of P. napi and P. rapae initiated throughout the season. The prediction that partial second generations should be female biased was corroborated by laboratory rearings at constant temperature of P. napi (Pieridae), Polygonia c-album (Nymphalidae), and Pararge aegeria (Satyridae) under critical day length conditions, producing female-biased sex ratio under direct, and male-biased sex ratio under diapause development.     

ESS emergence pattern of male butterflies in stochastic environments

Summary The evolutionarily stable (or ESS) emergence schedule for males of univoltine butterflies is analysed in an environment in which the female emergence schedule fluctuates stochastically between years. The ESS emergence curve, computed using the mutant invadability criterion, is shown to be the one that maximizes mean logarithmic lifetime mating success in the population in which it dominates. If males have accurate information about the female emergence schedule within each year, their emergence curve would evolve to the one predicted by a deterministic game model. The male emergence curve would then shift between years, closely following year to year changes in the female emergence pattern. If, instead, males have uncertainty about the female emergence schedule, the ESS male emergence curve becomes broader than the one predicted by the deterministic game model and will not track the between-year fluctuation of female emergence well. In a special case, we show how the between-year variation of mean emergence date, the variance of emergence date, the sexual difference in mean emergence dates (protandry) and the between-year correlation of mean emergence dates of both sexes should change with the degree of accuracy of information available to males.     

Ladies last: diel rhythmicity of adult emergence in a parasitoid with complementary sex determination

Protandry, the earlier adult emergence of males, is explained as either an adaptive strategy maximizing male mating opportunities at the same time as minimizing female pre‐reproductive mortality, or as an incidental by‐product of sexual dimorphism fuelled by selection for other life‐history traits. Adult emergence sequences are monitored of broods of the gregarious larval endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) undergoing pupal development under different temperature regimes. As a haplodiploid species with single‐locus complementary sex determination, gender in C. glomerata is determined by the genotype at one sex locus. Haploids are always male, whereas diploids are female when heterozygous but male when homozygous at the sex locus. Sibling mating promotes homozygosity and thus the production of diploid males. Diploid males are produced at the expense of females, and impose a genetic burden on individuals and populations, despite their exceptional fertility in C. glomerata. Emergence of broods is typically completed within 2 days. Irrespective of temperature, males emerge earlier and within a shorter time interval than females, and a majority of the males in a cluster emerge before the first female. The implications of an incomplete temporal segregation of the sexes on the incidence of inbreeding in C. glomerata are discussed in the light of its sex determination mechanism and its patterns of mating, host exploitation and natal dispersal.     

Models for the evolution of protandry in insects

Protandry is the tendency for males to emerge before females, and it is common in insects with discrete, nonoverlapping generations in which females mate once only soon after emergence. In these circumstances males which emerge early will have more opportunities to mate than those which emerge late, so that protandry would be expected to evolve through sexual selection. In diploid species in which the primary sex ratio is fixed, protandry can evolve only through shortening the developmental time of males, so changing the distribution of their emergence times. Two models of the evolution of protandry in this way are compared. The first model assumes that the distribution of male emergence times can respond without any constraint to sexual selection, so leading to an “ideal free” distribution; the second model assumes that the distribution can shift only in mean (or possibly in mean and variance), but not in shape.     

A game model for the daily activity schedule of the male butterfly

A game model is developed of the daily schedule of matesearching activity by male butterflies, assuming that each male maximizes his expected mating success given a limited total time for mate search. The model predicts that (1) in the early morning, no male is active even though many females are emerging; (2) at a critical time, many males suddenly become active; and (3) the male's maximum activity occurs after the peak female emergence and before the peak capture efficiency. The inverse problem is also analyzed, in which the temporal pattern of capture efficiency is estimated from the knowledge of male activity and female emergence, assuming the evolutionarily stable strategy (ESS) condition. The model is then applied to data from a cabbage white butterfly (Pieris rapae crucivora) population and predicts that (1) females remain unmated for several hours on average after emergence, and (2) the male 's capture efficiency is rather low and increases significantly with time during the morning.     

Mating opportunity and the evolution of sex-specific mortality rates in a butterfly

Life history theory predicts that organisms should only invest resources into intrinsic components of life span to the degree that it pays off in terms of reproductive success. Here, we investigate if the temporal distribution of mating opportunities may have influenced the evolution of intrinsic mortality rates in the butterfly Pararge aegeria (Satyrinae). In this species, females mate only once and the frequency of male mating opportunities depends on the temporal emergence pattern of virgin females. As expected, in a population from Madeira where females emerge continuously throughout the year, there was no sex difference in adult life span, while in a Swedish population with synchronised female emergence, males had significantly shorter life spans compared to females. A logistic mortality model provided the best fit to the observed change in age-specific mortality and all categories reached an asymptotic mortality rate of a similar magnitude. However, the Swedish males reached this mortality plateau more rapidly than the other categories. External mortality, due to water and food limitation, affected the pattern of sex-specific mortality but males from Sweden still had higher rates of mortality compared to all other categories. We argue that selection on male longevity is likely to be weaker in Sweden because under synchronised emergence, all females emerge and mate within a short period of time, after which male reproductive value will quickly approach zero. On Madeira, however, male reproductive value decrease more slowly with age since the probability of finding a receptive female is constant over the year. Received: 29 July 1999 / Accepted: 23 August 1999     

High Female Survival Promotes Evolution of Protogyny and Sexual Conflict

Existing models explaining the evolution of sexual dimorphism in the timing of emergence (SDT) in Lepidoptera assume equal mortality rates for males and females. The limiting assumption of equal mortality rates has the consequence that these models are only able to explain the evolution of emergence of males before females, i.e. protandry—the more common temporal sequence of emergence in Lepidoptera. The models fail, however, in providing adaptive explanations for the evolution of protogyny, where females emerge before males, but protogyny is not rare in insects. The assumption of equal mortality rates seems too restrictive for many insects, such as butterflies. To investigate the influence of unequal mortality rates on the evolution of SDT, we present a generalised version of a previously published model where we relax this assumption. We find that longer life-expectancy of females compared to males can indeed favour the evolution of protogyny as a fitness enhancing strategy. Moreover, the encounter rate between females and males and the sex-ratio are two important factors that also influence the evolution of optimal SDT. If considered independently for females and males the predicted strategies can be shown to be evolutionarily stable (ESS). Under the assumption of equal mortality rates the difference between the females’ and males’ ESS remains typically very small. However, female and male ESS may be quite dissimilar if mortality rates are different. This creates the potential for an ‘evolutionary conflict’ between females and males. Bagworm moths (Lepidoptera: Psychidae) provide an exemplary case where life-history attributes are such that protogyny should indeed be the optimal emergence strategy from the males’ and females’ perspectives: (i) Female longevity is considerably larger than that of males, (ii) encounter rates between females and males are presumably low, and (iii) females mate only once. Protogyny is indeed the general mating strategy found in the bagworm family.     

Synchronization of reproductive period among the two male forms and female of the damselflyMnais pruinosa selys (Zygoptera: Calopterygidae)

Ecological parameters in a population ofMnais pruinosa were investigated in a mountain stream. In the study area, there were two forms of male with regard to wing color, the orange-winged male (esakii) and the hyaline-winged male (strigata), and only one female form with hyaline wings. Emergence of adults began in late April, and the flying season ended in late June. The time after emergence was spent in maturation, and the insects began to mate when they reached maturity. Longevity of adults was 17.6 days foresakii males, 18.4 days forstrigata males and 21.9 days for females. There was little difference in emergence time, maturation period, survivorship curve and longevity among the two male forms and female. In other words, the period for reproductive activities was perfectly coincident among them. The factors influencing the synchronization of emergence were discussed.     

Male emergence timing and mating success in the funnel-web spider,Agelena limbata (Araneae: Agelenidae)

Field observations on the relationship between male mating success and emergence timing in the funnel-web spider,Agelena limbata, were conducted.Agelena limbata is an annual species and adult males appear slightly earlier than adult females in July. As males deposit a copulatory plug at the female epigynum after copulation, copulation with virgin females is important to males. The number of copulations in males with virgin females, which strongly correlates with the longevity of males and the number of females that males courted, did not correlate with the emergence timing of males. Early emerged males and females were significantly larger in size than later ones, but the correlation coefficient between the emerged date and the cephalothorax width was not strong. Males that emerged earlier did not have any advantage in copulating with larger and more fecund females. Furthermore, virgin females first copulated on average 7.9 days after their final molt and the mortality rate of adult males increased after the final molt. These factors may favor the smaller degree of protandry in male emergence timing inA. limbata.     

Differences in response to defoliation between males and females of Silene dioica

Summary The response by male and female plants to herbivory was studied by experimental defoliation of the dioecious perennial herb Silene dioica in a green-house. Male and female plants were defoliated prior to and during the early flowering phase at two intensities (50% and 100% of leaf-area removed) in two consecutive years. Defoliation resulted in a decrease in the number of flowers initiated in both sexes, while a larger delay of peak flowering and a higher mortality was observed in males compared to females. In female plants, severe defoliation resulted in a reduction in seed number per capsule and in seed size compared to control. Females showed a negative correlation between the production of flowers in the first and second season in all treatments, while flowering in males the first season was not correlated with flowering in the second season. Females also showed a lower frequency of flowering than males during the two seasons studied. However, during the flowering period, males allocated significantly more biomass to flowers than did females. This outcome supports the idea that females may have a higher total reproductive expenditure than males, but males have a higher reproductive effort during flowering. Male rosette leaves were significantly preferred by the generalist herbivore Arianta arbustorum in experiments. This preference was most pronounced in trials with leaves from fertilized plants compared to nonfertilized plants. A greater storage of resources in aboveground leaves during winter by males compared to females may explain the higher preference for male leaves and the higher male mortality following early defoliation. Furthermore, males are smaller than females and may have a lower ability than females to replace lost resources needed for reproduction when defoliated early in the season.     

Impact of the Timing of Male Emergence on Mating Capacity of Males in Trichogramma evanescens Westwood

In species with highly structured population, such as Trichogramma spp., mating occurs mostly at emergence on the patch and early emerging males have an advantage, as they are present when the first females emerge. However, early emergence of male could also enable males to mature sexually before the emergence of females or enhance their capacity to induce higher receptivity in females. We measured time of emergence of male and female Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) from hosts that were parasitized within a 30 min period. We also measured the effect of male age on their capacity to mate, and the ability of inseminated females to produce daughters. To verify if early emerging males induced higher receptivity in females, we observed the females mate choice between males of different ages. Our results indicated that the mean time of emergence between males and females was 29 min for individuals that develop in 9 days and 10 min for individuals that develop in 10 days. The protandry observed in this species could be the result of either a faster development of males or a male first strategy by the ovipositing female. In T. evanescens, protandry does not permit males to mature sexually nor to induce higher receptivity in females. The main advantage of protandry for males thus appears to be early access to females as they emerge.     

Changing seasonality and phenological responses of free-living male arctic ground squirrels: the importance of sex

Many studies have addressed the effects of climate change on species as a whole; however, few have examined the possibility of sex-specific differences. To understand better the impact that changing patterns of snow-cover have on an important resident Arctic mammal, we investigated the long-term (13 years) phenology of hibernating male arctic ground squirrels living at two nearby sites in northern Alaska that experience significantly different snow-cover regimes. Previously, we demonstrated that snow-cover influences the timing of phenological events in females. Our results here suggest that the end of heterothermy in males is influenced by soil temperature and an endogenous circannual clock, but timing of male emergence from hibernation is influenced by the timing of female emergence. Males at both sites, Atigun and Toolik, end heterothermy on the same date in spring, but remain in their burrows while undergoing reproductive maturation. However, at Atigun, where snowmelt and female emergence occur relatively early, males emerge 8 days earlier than those at Toolik, maintaining a 12-day period between male and female emergence found at each site, but reducing the pre-emergence euthermic period that is critical for reproductive maturation. This sensitivity in timing of male emergence to female emergence will need to be matched by phase shifts in the circannual clock and responsiveness to environmental factors that time the end of heterothermy, if synchrony in reproductive readiness between the sexes is to be preserved in a rapidly changing climate.     

Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success

Many organisms with complex life cycles show considerable variation in size and timing at metamorphosis. Adult males of Megarcyssignata (Plecoptera: Perlodidae) are significantly smaller than females and emerge before females (protandry) from two western Colorado streams. During summer 1992 stoneflies from a trout stream emerged earlier in the season and at larger sizes than those from a colder fishless stream, and size at metamorphosis did not change over the emergence period in either stream. We performed two experiments to determine whether variation in size at metamorphosis affected the fecundity, reproductive success and longevity of individuals of this stonefly species and if total lifetime fecundity was affected by the number of matings. In the first experiment, total lifetime fecundity (eggs oviposited) was determined for adult females held in small plastic cages in the field. Males were removed after one copulation, or pairs were left together for life and allowed to multiply mate. Most copulations occurred in the first few days of the experiment. Females in treatments allowing multiple matings had significantly lower total lifetime fecundity and shorter adult longevity than females that only mated once. Multiple matings also reduced longevity of males. Fecundity increased significantly with female body mass at emergence, but only for females that mated once. While multiple matings eliminated the fecundity advantage of large female body size, number of matings did not affect the significant positive relationship between body mass at metamorphosis and longevity of males or females. In a second experiment designed to determine if body mass at emergence affected male mating success, we placed one large and one small male Megarcys in an observation arena containing one female and recorded which male obtained the first mating. The large and the small male had equal probabilities of copulating with the female. Copulations usually lasted all night, and the unmated male made frequent, but unsuccessful attempts to take over the copulating female. Our data suggest that selection pressures determining body size at metamorphosis may operate independently on males and females, resulting in evolution of sexual size dimorphism, protandry, and mating early in the adult stage. We emphasize the importance of interpreting the fitness consequences of larval growth and development on the timing of and size at metamorphosis in the context of the complete life cycle. Received: 1 July 1997 / Accepted: 12 November 1997     

A new type of male dimorphism with ergatoid and short-winged males in Cardiocondyla cf. kagutsuchi

Summary. A new type of ant male dimorphism, consisting of wingless (ergatoid) and short-winged (brachypterous) males, was found in a species of the “Cardiocondyla kagutsuchi”- complex from Malaysia. The ergatoid males show the typical morphological and behavioral characteristics of those of many other Cardiocondyla species. The brachypterous males are morphologically intermediate between ergatoid males and typical winged males of other taxa in this genus. On one hand, they share a number of morphological and behavioral features with ergatoid males that might be adaptations to the loss of flight and intranidal mating: aggressive behavior towards rival males, a prolonged spermatogenesis, which is unique in winged males, paler body coloration, smaller compound eyes, shorter antennal funiculi, more rounded heads – perhaps due to the increased development of mandibular muscles, and an angular pronotum, probably for neck protection. Their short wings appear to protect the petiolar joints during fighting. On the other hand, the brachypterous males have not become as specialized as the ergatoids and to some extent keep the nature of the winged males of other species, i.e., they escape from the nest with a higher probability and with less injuries and do not show a reduction of the ocelli. In the sexual production season, the ergatoid males emerged first in small numbers and then both male morphs emerged in large numbers. The sex ratio was extremely female-biased in the earlier stage of sexual production, probably due to local mate competition.Received 13 December 2004; revised 17 February 2005; accepted 22 February 2005.     

Small males emerge earlier than large males in Dawson's burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini)

Females of Dawson's burrowing bee ( Amegilla dawsoni ) are receptive to the males as they emerge but have become unreceptive by the time they begin to nest. In addition, there is a single emergence period per year lasting about a month. These factors are predicted to lead to protandry and males of Dawson's burrowing bee do tend to emerge earlier in the annual flight season than females. Moreover, even during a single day, emerging males tend to precede females. The degree of protandry, however, is size-dependent, with smaller males tending to precede larger ones, both over the course of the flight season and on any given day. Because small males are at a disadvantage in the fights that occur for females, the earlier emergence of minor males may be a sexually selected response that reduces the likelihood that they will be displaced from potential mates by larger rivals.     

NATURAL SELECTION AND SEXUAL SIZE DIMORPHISM IN RED-WINGED BLACKBIRDS

Patterns of overwinter mortality in the sexually dimorphic red-winged blackbird (Agelaius phoeniceus) were examined to test the predictions of the sexual-selection hypothesis that male size is limited by directional selection favoring small males and that female size is maintained by stabilizing selection wherein extreme phenotypes experience higher mortality. Museum specimens collected from Ontario over a 95-yr period were used to compare the sizes of males and females collected in fall and spring. In a separate field study, body sizes of returning and nonreturning male and female red-winged blackbirds were compared over a 6-yr period. Overall, there was no evidence of higher overwinter mortality among larger males. Among adult (ASY) males, large individuals appeared to have higher survival than small individuals, although among subadult (SY) males, large size may have been disadvantageous. Weak evidence of stabilizing selection on female body size was found. Among adults, sexual size dimorphism seemed more pronounced after winter than before winter. Our results do not support the hypothesis that body size in male red-winged blackbirds is limited by selective mortality outside the breeding season. It is possible that size selection occurs earlier in life, when males are still in the nest. Our results suggest that caution should be exercised when interpreting interspecific evidence showing higher adult male than female mortality in sexually dimorphic species. Such patterns could arise as a cost to males of sexual selection and yet provide no insight into how natural selection opposes sexual selection for increased male size.     

Variation in the Boldness of Courting Sand Fiddler Crabs (Uca pugilator)

Individuals can express boldness in their readiness to resume courtship signaling following a perceived threat. The degree of boldness that is selectively favored depends on the magnitude of costs and benefits that may vary across time and space. We examined within‐ and between‐individual variation in the boldness of courting male sand fiddler crabs, Uca pugilator, across an entire breeding season at a South Carolina (USA) salt marsh where courtship is restricted to supratidal embankments. Boldness was assessed by the time to re‐emergence and the number of re‐emergences of males who were purposely startled into their breeding burrows once every 3 min for a total of five times. The two measures of boldness were significantly positively correlated. Courting males are on average bolder when their density is high and when tidal conditions correspond to peaks in the number of females moving over the embankment surface. Time to re‐emergence increases with successive startles although some males consistently re‐emerge faster than others. Large males are not bolder than small males. When male density is high, nearest neighbors frequently re‐emerge at the same time, suggesting that males cue on the responses of other nearby males, perhaps by assessing substrate vibration. This may reduce the chance of losing a potential mate to a local competitor.     

A two‐step mechanism controls the timing of behaviour leading to emergence from soil in adult males of the scarab beetle Dasylepida ishigakiensis

Adults of the white grub beetle Dasylepida ishigakiensis Niijima et Kinoshita (Coleoptera: Scarabaeidae) emerge from the soil around dusk for mating on subtropical islands. The present study examines the factors controlling the emergence of males in the laboratory. There are two steps involved. Standby behaviour (i.e. insect head appears at the soil surface) can be observed for several hours before the beetles actually emerge for mating. The standby behaviour is facilitated by warm conditions, although the proportion of standby individuals is influenced not only by the temperature on that day, but also by that on the previous day. Experiments in which beetles are exposed to photoperiod and thermoperiod combinations, in and out of phase, show that temperature is more important in inducing standby and emerging behaviour than light alone. For the second step, factors such as temperature, light and the presence of the female sex pheromone determine whether males will leave the standby position and emerge onto the ground. The female sex pheromone stimulates standby beetles to exhibit emerging and wing vibration behaviours, although the effect depends on when it is presented to beetles. Beetles burrow back into the soil; this behaviour is influenced by illumination and time of the day but not by temperature. The results suggest that D. ishigakiensis possesses a sophisticated mechanism controlling male emergence from the soil.     

Temporal Variation in the Sex Ratio of a Natural Population of a Multivoltine Gall-Inducing Braconid Wasp

Temporal variation in the sex ratio of populations with continuous generations is poorly understood. We report changes in the sex ratio of a tropical gall-inducing braconid wasp throughout the fruiting season of its host plant. At the beginning of the season, fruits produce male biased sex ratios; at the end, female biased sex ratios. This change results from differential sex allocation rather than just earlier male emergence. A male bias followed by female bias is predicted following an increase in recruitment as occurs during the start of the main fruiting season, because males are likely to have the more consistent reproductive value over time. An initial male bias might also result from selection for protandry, or from constrained sex allocation during the low-density non-fruiting season.     

Adult life and emergence of Dolania americana in Northwestern Florida (Ephemeroptera: Behningiidae)

The adult habits and emergence of Dolania americana (Ephemeroptera: Behningiidae) were studied at the Blackwater River in Northwestern Florida. The adult life is crepuscular, beginning about 1½ hrs before sunrise with emergence of male subimagos. Males molt to imagos, female subimagos emerge, males and females mate, and females begin to oviposit in a fairly precise time sequence over the following hour. Only a few adults survive past sunrise. Females never molt to imagos and are polymorphic. Emergence is seasonal and begins between the end of April and the middle of May, depending on climatic conditions. Emergence is photoperiodically entrained. Water temperature is a phase setter and light intensity acts as a synchronizer.