Physiological Costs of Mate Guarding in the Japanese Beetle (Popillia japonica Newman)

Males of many insects directly defend their mates from rival males (i.e. mate guard) as a way to avoid sperm competition and thus increase their reproductive success. However, mate guarding may have associated costs for these males. We examined costs of mate guarding in Japanese beetles (Popillia japonica), a pest species which exhibits post‐copulatory mate guarding during which the guarding male cannot feed. In this species, food provides both energy and water for thermoregulation. Consequently, we focused on possible thermoregulatory and energetic costs of their mate guarding. In a field study, we found that guarding males had significantly higher thoracic temperatures than non‐guarding males, indicating a difference in their ability and/or need to thermoregulate. Paired males had significantly lower water levels than single males in the morning and evening, but not in the afternoon. In the laboratory, we found that mate‐guarding duration was significantly shorter at higher ambient temperature than at lower temperature, and males that had been starved guarded for less time than males that had not been starved. Our results suggest that because guarding males are unable to feed, they suffer energetic and thermoregulatory costs that appear to limit the amount of time that they can guard a female.     

Greater opportunities for sexual selection in male than in female obligate brood parasitic birds

Females are expected to have evolved to be more discriminatory in mate choice than males as a result of greater reproductive investment into larger gametes (eggs vs. sperm). In turn, males are predicted to be more promiscuous than females, showing both a larger variance in the number of mates and a greater increase in reproductive success with more mates, yielding more intense sexual selection on males vs. females (Bateman's Paradigm). However, sex differences in costly parental care strategies can either reinforce or counteract the initial asymmetry in reproductive investment, which may be one cause for some studies failing to conform with predictions of Bateman's Paradigm. For example, in many bird species with small female‐biased initial investment but extensive biparental care, both sexes should be subject to similar strengths of sexual selection because males and females are similarly restricted in their ability to pursue additional mates. Unlike 99% of avian species, however, obligate brood parasitic birds lack any parental care in either sex, predicting a conformation to Bateman's Paradigm. Here we use microsatellite genotyping to demonstrate that in brood parasitic brown‐headed cowbirds (Molothrus ater), per capita annual reproductive success increases with the number of mates in males, but not in females. Furthermore, also as predicted, the variance of the number of mates and offspring is greater in males than in females. Thus, contrary to previous findings in this species, our results conform to predictions of the Bateman's Paradigm for taxa without parental care.     

Song and Sperm in Crickets: A Trade‐off between Pre‐ and Post‐copulatory Traits or Phenotype‐Linked Fertility?

When females mate multiply (polyandry) both pre‐ and post‐copulatory sexual selection can occur. Sperm competition theory predicts there should be a trade‐off between investment in attracting mates and investment in ejaculate quality. In contrast, the phenotype‐linked fertility hypothesis predicts a positive relationship should exist between investment in attracting mates and investment in ejaculate quality. Given the need to understand how pre‐ and post‐copulatory sexual selection interacts, we investigated the relationship between secondary sexual traits and ejaculate quality using the European house cricket, Acheta domesticus. Although we found no direct relationship between cricket secondary sexual signals and ejaculate quality, variation in ejaculate quality was dependent on male body weight and mating latency: the lightest males produced twice as many sperm as the heaviest males but took longer to mate with females. Our findings are consistent with current theoretical models of sperm competition. Given light males may have lower mating success than heavy males because females take longer to mate with them in no‐choice tests, light males may be exhibiting an alternative reproductive tactic by providing females with more living sperm. Together, our findings suggest that the fitness of heavy males may depend on pre‐copulatory sexual selection, while the fitness of light males may depend on post‐copulatory fertilization success.     

Do males choose their mates in the lekking moth Achroia grisella? Influence of female body mass and male reproductive status on male mate choice

Lekking males aggregate to attract females and contribute solely to egg fertilization, without any further parental care. Evolutionary theory therefore predicts them to be nonchoosy toward their mates, because any lost mating opportunities would outweigh the benefits associated with such preferences. Nevertheless, due to time costs, the production of energetically costly sexual displays, and potential sperm limitation, the mating effort of lekking males is often considerable. These factors, combined with the fact that many females of varying quality are likely to visit leks, could favor the evolution of male mate preferences. Here, we show that males of the lekking lesser wax moth, Achroia grisella, were indeed more likely to mate with heavier females in choice experiments, even at their virgin mating (i.e., when their reproductive resources have not yet been depleted by previous matings). This differential female mating success could not be attributed to female behavior as heavy and light females showed similar motivation to mate (i.e., latency to approach the males) and time to copulate. Males seem to benefit from mating with heavier females, as fecundity positively correlated with female mass. This new empirical evidence shows that male mate choice may have been underestimated in lekking species.     

Mate fidelity in a polygamous shorebird,the snowy plover (Charadrius nivosus)

Social monogamy has evolved multiple times and is particularly common in birds. However, it is not well understood why some species live in long‐lasting monogamous partnerships while others change mates between breeding attempts. Here, we investigate mate fidelity in a sequential polygamous shorebird, the snowy plover (Charadrius nivosus), a species in which both males and females may have several breeding attempts within a breeding season with the same or different mates. Using 6 years of data from a well‐monitored population in Bahía de Ceuta, Mexico, we investigated predictors and fitness implications of mate fidelity both within and between years. We show that in order to maximize reproductive success within a season, individuals divorce after successful nesting and re‐mate with the same partner after nest failure. Therefore, divorced plovers, counterintuitively, achieve higher reproductive success than individuals that retain their mate. We also show that different mating decisions between sexes predict different breeding dispersal patterns. Taken together, our findings imply that divorce is an adaptive strategy to improve reproductive success in a stochastic environment. Understanding mate fidelity is important for the evolution of monogamy and polygamy, and these mating behaviors have implications for reproductive success and population productivity.     

Mendel’s law reveals fatal flaws in Bateman’s 1948 study of mating and fitness

Bateman’s experimental study of Drosophila melanogaster produced conclusions that are now part of the bedrock premises of modern sexual selection. Today it is the most cited experimental study in sexual selection, and famous as the first experimental demonstration of sex differences in the relationship between number of mates and relative reproductive success. We repeated the experimental methodology of the original to evaluate its reliability. The results indicate that Bateman’s methodology of visible mutations to assign parentage and reproductive success to subject adults is significantly biased. When combined in offspring, the mutations decrease offspring survival, so that counts of mate number and reproductive success are mismeasured. Bateman’s method overestimates the number of subjects with no mates and underestimates the number with one or more mates for both sexes. Here we discuss why Bateman’s paper is important and present additional analyses of data from our monogamy trials. Monogamy trials can inform inferences about the force of sexual selection in populations because in monogamy trials male–male competition and female choice are absent. Monogamy trials also would have provided Bateman with an a priori test of the fit of his data to Mendel’s laws, an unstated, but vital assumption of his methodology for assigning parentage from which he inferred the number of mates per individual subject and their reproductive success. Even under enforced monogamous mating, offspring frequencies of double mutant, single mutant and no mutant offspring were significantly different from Mendelian expectations proving that Bateman’s method was inappropriate for answering the questions he posed. Double mutant offspring (those with a mutation from each parent) suffered significant inviability as did single mutant offspring whenever they inherited their mother’s marker but the wild-type allele at their father’s marker locus. These inviability effects produced two important inaccuracies in Bateman’s results and conclusions. (1) Some matings that actually occurred were invisible and (2) reproductive success of some mothers was under-estimated. Both observations show that Bateman’s conclusions about sex differences in number of mates and reproductive success were unwarranted, based on biased observations. We speculate about why Bateman’s classic study remained without replication for so long, and we discuss why repetition almost 60 years after the original is still timely, necessary and critical to the scientific enterprise. We highlight overlooked alternative hypotheses to urge that modern tests of Bateman’s conclusions go beyond confirmatory studies to test alternative hypotheses to explain the relationship between mate number and reproductive success.     

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics

In socially monogamous species, mate‐guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate‐guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate‐guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate‐guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry. Am. J. Primatol. 72:942–950, 2010. © 2010 Wiley‐Liss, Inc.     

Seasonal Variation in Mate Choice of Photinus ignitus Fireflies

Mate choice by either sex may vary with changes in the associated costs and benefits, determined by factors such as the availability of potential mates and variation in mate quality. We examined seasonal variation in operational sex ratio, courtship behavior, spermatophore mass, egg count, and the relationship between morphological traits and mating success in Photinus ignitus fireflies to determine if mate choice in either sex varied with the availability and relative reproductive investment of fertilizable females and sexually active males. Successfully mating males had larger lanterns than unsuccessful males when the operational sex ratio was male‐biased. In addition, female responsiveness to male signals increased as the number of courting males decreased, and male spermatophore mass decreased with body size across the mating season. Successfully mating females had larger body mass than unsuccessful females. Female body mass predicted egg count and female rejection by males increased as the season progressed and female size decreased. These results suggest that both male and female P. ignitus exhibit mate choice, and that such choice is influenced by seasonal variation in the abundance and quality of potential mates.     

Mate Guarding in the Androdioecious Clam Shrimp Eulimnadia texana: Male Assessment of Hermaphrodite Receptivity

Precopulatory mate guarding primarily occurs when males encounter receptive females at a low enough rate that such females become a valuable resource once encountered. Such circumstances are common in aquatic crustaceans wherein females are only receptive for a short period directly after molting. In these species, males commonly mate guard by physically attaching themselves to their prospective mates for hours to days at a time. To be effective in mate guarding, males must be able to assess the time to receptivity in their mates, which is commonly via chemical cues associated with molting. Clam shrimp in the genus Eulimnadia exhibit mate guarding, but with an important variation: these species are mixtures of males and hermaphrodites (androdioecy) rather than males and females. Nonetheless, the mate guarding behaviors of these shrimp are much the same as in other aquatic crustaceans. In this study, three projects were undertaken to determine the ability of Eulimnadia texana males to assess hermaphroditic receptivity. Males were found to be unable to assess receptivity without physically contacting hermaphrodites. However, after physical contact, males spent a significantly greater amount of time guarding receptive relative to non‐receptive hermaphrodites. Additionally, male interest in mate guarding was highest during the period between the dropping of one clutch of eggs and the extrusion of the following clutch. Because this period is also associated with hermaphroditic molting, it is consistent with the notion that males cue into chemicals associated with molting to determine hermaphroditic receptivity. These findings are consistent with previous studies of mating behavior in this species, and we discuss their importance to future tests of optimal mate guarding planned for these shrimp.     

Age-Related Variation in Mate-Guarding Intensity in the Bluethroat (Luscinia s. svecica)

Female extra‐pair copulations (EPCs) have selected for male paternity guarding strategies in many bird species. In the bluethroat, Luscinia s. svecica, males guard their mates closely during the last 2 d before the start of egg laying, but there is great individual variation in the intensity of mate guarding. Here we show that some of this variation is related to male age. Old males guarded their mates with much lower intensity and sang more than young males, although the latter difference was not statistically significant. Controlling for male age, male and female coloration and size were not significantly related to the intensity of mate guarding. We have previously shown that young and old males had a similar paternity loss in their own broods. On the other hand, old males were far more successful than young males in achieving extra‐pair fertilizations. These patterns suggest that young and old males have different trade‐offs between preventing paternity loss in own nest and gaining paternity in others, because male skills in obtaining EPCs improve with experience and/or because of female preferences for old males as copulation partners. There were no significant relationships between paternity and male mate‐guarding behaviour during the fertile period, indicating that mate guarding is not a very effective paternity‐assurance strategy in the bluethroat.     

FEMALE REPRODUCTIVE EFFORT DEPENDS ON THE DEGREE OF ORNAMENTATION OF THEIR MATES

Sexual selection theory assumes that secondary sexual characters do not influence female reproductive effort. Female animals may invest relatively more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred males may be relatively more viable than offspring sired by less preferred males. Here we report for the first time in a field study that females of the monogamous barn swallow Hirundo rustica adjust their reproductive effort to the attractiveness of their mates. Experimental manipulation of male tail length, which is a trait currently subject to a directional female mating preference, affected the reproductive effort by females in single broods as well as their decision on the seasonal number of clutches. These results, and those of previous experiments, demonstrate that female barn swallows assess the quality of their mates throughout the reproductive season and adjust their reproductive decisions accordingly. This result has important implications for the theory of sexual selection and for the possibility of testing current models of female mate preferences, because the viability of offspring will be confounded by differential reproductive effort.     

Interspecific differences in male cannibalistic behavior between two sympatric cardinalfishes (Pisces: Apogonidae)

Cannibalistic behavior of a paternal mouthbrooding cardinalfish, Apogon notatus, was examined and compared with that of a sympatric congener, Apogon doederleini. In both species, males sometimes cannibalized their own entire broods, but their postcannibalistic behavior was markedly different. Males of A. doederleini respawned within a few days of cannibalism, usually changing mates, whereas males of A. notatus took several weeks to respawn, less frequently changing mates. This difference was attributed to mate availability for males. The operational sex ratio was female biased in A. doederleini but male biased in A. notatus, suggesting that the former males have higher mate availability and thus opportunities for remating soon after cannibalism. For male apogonids that accept only one clutch at a time, an effective way to compensate for reproductive loss entailed by filial cannibalism is to remate as soon as possible after cannibalism. The higher rate of filial cannibalism by A. doederleini than by A. notatus suggests that this cannibalism is facilitated by high mate availability. In contrast to filial cannibalism, heterocannibalism was more frequent in A. notatus. High population density and gregariousness may be important factors contributing to the frequent occurrence of heterocannibalism. Received: January 6, 1999 / Accepted: May 14, 1999     

The Influence of Age on Male Mate‐Searching Behaviour in Thornbug Treehoppers

One prediction from life‐history theory is that males should increase investment in reproductive effort as they age because the opportunity for future reproductive events declines. However, older males may not be able to increase their reproductive effort if condition declines with age. The effect of age‐related changes in condition may be especially important for energetically costly activities such as moving within and between habitat patches while searching for mates. Although such searching is a component of many mating systems, the relationship between age and active mate searching has not been investigated. We investigated whether mate‐searching effort increased with age in the thornbug treehopper, Umbonia crassicornis (Hemiptera: Membracidae). In this species, males search for females using a ‘fly‐call‐walk’ strategy consisting of three phases: (1) flying from one plant to another; (2) walking and signalling while on a plant; and (3) close‐range courtship of encountered females. We measured several aspects of mate‐searching behaviour over the month‐long period of a male’s reproductive lifetime. Over the relevant period of male sexual activity (19–33 d), male condition remained stable. However, older males (25–33 d) did not search more actively than younger males as predicted; instead, younger males (19 d) had greater plant‐to‐plant flight activity and found females faster. Within‐plant walking rates and courtship duration did not differ among age classes. These results suggest that thornbug males may be investing so heavily in mate searching at younger ages that they are unable to increase investment in searching effort when they get older. As a result, older males are likely to be at a competitive disadvantage when active searching is required to locate sparsely distributed females.     

Male and Female Soldier Beetles Relax Choice for Mate Quality Across Daily Courtship Periods

Mutual mate choice occurs when members of each sex will reject some potential mates in efforts to encounter better prospects later. The decision to reject may represent the interaction between mate preferences, mate availability, and temporal constraints. Theory predicts that mutual mate choice will favor relaxed choosiness as mate availability and time for courtship decline. We explored mutual mate choice in the soldier beetle, Chauliognathus pennsylvanicus (Cantharidae), where courtship consisted of males attempting to secure evasive females. We employed field observations, laboratory experiments, and stochastic simulations to investigate the decline in choosiness over the daily courtship period, during which individuals can mate at most once. We found that reproductive success of males and females increases with mate size and mating frequency. Females biased copulations toward larger mates by attempting to evade suitors, while males biased copulations by releasing the smaller females they capture. However, late in the day males and females may increase reproductive success by accepting rather than rejecting lower quality mates to maintain high mating rates. Stochastic simulations indicated that reproductive success, the product of mating frequency and mean mate size, was maximized in males and females by incrementally reducing mate standards across daily courtship periods. In the field, large males who rejected small females early in the daily courtship period rarely did so later. Large females used less effective evasive maneuvers later in the courtship period, resulting in copulations with progressively smaller males. These results support models of mutual mate choice that predict that individuals of high quality will maximize reproductive success by relaxing choosiness as the courtship period wanes.     

Dynamics of House Sparrow Biparental Care: What Contexts Trigger Partial Compensation?

Nest attendance during incubation is characterized by an inequitable division of labor in house sparrows, Passer domesticus, with females spending more time at the nest than males. Previous research has shown that if male contributions are reduced experimentally via testosterone (T) implants, females compensate partially for those reductions, consistent with predictions from most models of negotiated biparental care. In this study, we attempted to identify the cues and contexts generating partial compensation, using data from both unmanipulated parents and pairs with T‐males. Both males and females of this species sometimes leave the nest before their mate returns to relieve them, and we found that these unrelieved departures by unmanipulated individuals occur when partners are on lengthy recesses. Females compensated partially for long male recesses by marginally extending their bouts; most females also slightly reduced their next recess. By contrast, when males left before their mate returned, they left earlier than when they waited for the female. Neither males nor females adjusted their recess lengths after returning to the nest and discovering that their partner was absent. More pronounced changes in nest attendance of unmanipulated parents occurred in the context of ‘visits’, when individuals returned to the nest but then left without relieving their mate. Such visits effectively prolonged the bout of the on‐duty partner and extended the visitor’s recess. Analyses of behavior of T‐males and their mates revealed that T‐males had significantly longer recesses than control males, and that their mates, in turn, had elevated rates of unrelieved departures. T‐males also visited their on‐duty mates more often than control males, whereas female visits to T‐males were rare. Collectively, the predicted changes in female nest attendance associated with lengthy male recesses and male and female visits account reasonably well for the compensatory response of females paired to T‐males. The majority of female compensation was attributable to changes in visit behavior, however, suggesting that much of the negotiation over nest attendance in this species occurs during direct interactions between mates.     

Male‐skewed adult sex ratio,survival, mating opportunity and annual productivity in the Snowy Plover Charadrius alexandrinus

Sex differences in adult mortality may be responsible for male‐skewed adult sex ratios and male‐skewed parental care in some birds. Because a surplus of breeding males has been reported in serially polyandrous populations of Snowy Plover Charadrius alexandrinus, we examined sex ratio, early‐season nesting opportunities, adult survival and annual reproductive success of a Snowy Plover population at Monterey Bay, California. We tested the hypotheses that male adult survival was greater than female survival and that a sex difference in adult survival led to a skewed adult sex ratio, different mating opportunities and different annual productivity between the sexes. Virtually all females left chicks from their first broods to the care of the male and re‐nested with a new mate. As a result, females had time to parent three successful nesting attempts during the lengthy breeding season, whereas males had time for only two successful attempts. Among years, the median population of nesting Plovers was 96 males and 84 females (median difference = 9), resulting in one extra male per eight pairs. The number of potential breeders without mates during the early nesting period each year was higher in males than in females. Adult male survival (0.734 ± 0.028 se) was higher than female survival (0.693 ± 0.030 se) in top‐ranked models. Annually, females parented more successful clutches and fledged more chicks than their first mates of the season. Our results suggest that in C. alexandrinus a sex difference in adult survival results in a male‐skewed sex ratio, which creates more nesting opportunities and greater annual productivity for females than for males.     

The lifetime costs of increased male reproductive effort: courtship,copulation and the Coolidge effect

The reproductive effort that a male directs to a familiar female declines over time, suggesting decreasing marginal returns. But is this diminishing returns a function of increasing reproductive costs or decreasing benefits of sustained effort? Here, we use the restoration of male reproductive effort with unfamiliar females to differentiate the role of diminishing returns and lifetime costs of increased reproductive effort of male guppies. We kept males with familiar or unfamiliar females throughout their lives and manipulated their ability to either court or mate with females. We found that increased male reproductive effort with novel mates lead to an immediate trade‐off in the form of reduced foraging effort. Further, males able to mate with a series of unfamiliar females had lower lifetime growth, indicating the primary cost of male reproductive effort in guppies arises from copulation rather than courtship. The lifetime growth trade‐offs were significant only when males mated with unfamiliar mates, suggesting that male reproductive effort with familiar females declines before it is restricted by physical exhaustion. These findings provide some of the first evidence of longitudinal costs of increased male reproductive effort in a vertebrate.     

Telomere length is reflected by plumage coloration and predicts seasonal reproductive success in the barn swallow

Individuals differ in realized fitness but the genetic/phenotypic traits that underpin such variation are often unknown. Telomere dynamics may be a major source of variation in fitness traits because physiological telomere shortening depends on environmental and genetic factors and may impair individual performance. Here, we showed that, in a population of a socially monogamous, biparental passerine bird, the barn swallow (Hirundo rustica), breeding in northern Italy, telomere length (TL) of both adult males and females positively correlated with seasonal reproductive and fledging success, as expected because long telomeres are supposed to boost performance. Telomere length was correlated with sexually dimorphic coloration in both sexes, showing for the first time in any species that coloration reliably reflects TL and may mediate mutual mate choice, leading to the observed positive assortative mating for TL in the barn swallow. Thus, TL appears to be associated with variation in a major fitness trait and may be an ultimate target of mate choice, as individuals of both sexes can use coloration to adaptively choose high‐quality mates that possess long telomeres.     

No evidence for adjustment of maternal investment under alternative mate availability regimes

Using treatments that mimic high and low availability of reproductive males, it was found that female three‐spined sticklebacks Gasterosteus aculeatus, previously shown to adjust their mate choices when male mates were rare, did not alter their reproductive investment strategies. These results suggest that plasticity in investment is perhaps limited by physiological requirements or dependent on relatively extreme mate availability regimes. The probability of becoming reproductive, number of clutches per season (per female), initial clutch size and mass and the timing of reproduction were all independent of the experience a female had with mate availability. This suggests that pre‐copulatory plasticity in reproductive strategies may contribute more to variation in the strength and direction of sexual selection than reproductive investment in offspring.     

Mating behavior and sex change of the anemonefish,Amphiprion clarkii,in the temperate waters of southern Japan

Synopsis In the main habitat of the anemonefishes Amphiprion, their movements between host sea anemones are generally restricted because of the low population density of hosts and high predation pressures. On the contrary, movements of A. clarkii between hosts were usual in the present study area (temperate waters of southern Japan), where host anemones are abundant. The general social unit of the anemonefishes is an isolated group consisting of a monogamous breeding pair and a varying number of nonbreeders. In the present study area, however, monogamous pairs established territories almost contiguous to others and nonbreeders had home ranges on the outskirts of the pairs' territories. The high host population density allows A. clarkii to move between hosts for searching for mates and acquiring additional mates. Most pair bonds lasted for more than 6 months, but 13% of the pairs separated because of migration of a mate to another territory. Bigamy occasionally originated from a penetration into a territory of a breeder by a mated neighbor of the opposite sex after the former's mate loss. Among 18 males who had lost their mates, only 3 changed sex and others re-paired with immigrant females, migrated to unmated females' territories or invaded pairs' territories. In the present study area, sex change to female is not the best way for an unmated male to increase his future reproductive success because of a loss of time spent on sex change and an opportunity to re-pair with new mates larger than himself, but is adaptively maintained as the best of a bad situation for the unmated male.