Sex,cannibalism and sticklebacks

Summary Two closely related species of sticklebacks (Pisces:Gasterosteidae), breeding in the same site at the same time, showed different patterns of egg cannibalism. In Gasterosteus aculeatus the intensity of cannibalism was density-dependent and females were the most important cannibals. In G. wheatlandi cannibalism was not density-dependent and males ate more eggs than females. This study indicates that sex-specific patterns of cannibalism can differ widely between species despite their similar ecology, and it provides evidence inconsistent with a currently popular explanation for egg cannibalism.     

The interval between sexual encounters affects male courtship tactics in a desert-dwelling fish

Courtship displays are often important in determining male mating success but can also be costly. Thus, instead of courting females indiscriminately, males might be expected to adjust their signalling effort strategically. Theory, however, predicts that such adjustments should depend on the rate with which males encounter females, a prediction that has been subject to very little empirical testing. Here, we investigate the effects of female encounter rate on male courtship intensity by manipulating the time interval between sequential presentations of large (high quality) and small (low quality) females in a fish, the Australian desert goby Chlamydogobius eremius. Males that were presented with a small female immediately after a large female reduced their courtship intensity significantly. However, males courted large and small females with equal intensity if the interval between the sequential presentations was longer. Our results suggest that mate encounter rate is an important factor shaping male reproductive decisions and, consequently, the evolutionary potential of sexual selection.     

Threat-sensitive foraging by larval threespine sticklebacks (Gasterosteus aculeatus)

Summary The threat-sensitive predator avoidance hypothesis predicts that prey can assess the relative threat posed by a predator and adjust their behaviour to reflect the magnitude of the threat. We tested the ability of larval threespine sticklebacks to adjust their foraging in the presence of predators by exposing them to conspecific predators of various sizes and recording their foraging and predator avoidance behaviours. Larvae (<30 days post-hatch) displayed predator escape behaviours only towards attacking predators. At 3 weeks post-hatch larvae approached the predator after fleeing, a behaviour which may be the precursor to predator inspection. Larvae reduced foraging and spent less time in the proximity of large and medium-sized predators compared to small predators. The reduction in foraging was negatively correlated to the predator/larva size ratio, indicating that larvae increased their foraging as they increased in size relative to the predator. We conclude that larval sticklebacks can assess the threat of predation early in their ontogeny and adjust their behaviour accordingly.Correspondence to: J.A. Brown     

Egg cannibalism by sticklebacks: spite or selfishness?

Summary Although it is generally agreed that humans can be spiteful, there are few if any, unambiguous examples of spite by non-human animals. Data are presented suggesting that female threespine sticklebacks show spiteful behaviour. In the field, they seek out conspecific eggs to attack while largely ignoring those of a closely-related sympatric species, the blackspotted stickleback. This occurs despite the fact that the latter's nests are more abundant and less well protected. In the laboratory, female threespine sticklebacks attack the eggs of conspecifics more than those of blackspotted sticklebacks, those of sympatric conspecific females more than those of allopatric females, and older eggs more than younger ones. Because there was no evidence of greater energetic or nutritional advantages from eating conspecific rather than heterospecific eggs, or older eggs rather than younger ones, threespine sticklebacks may be spiteful. Alternative proximate and evolutionary hypotheses to explain this discriminant egg-eating are discussed.     

Predation risk affects courtship and attractiveness of competing threespine stickleback males

The effect of predation risk and male-male competition on male courtship behaviour and attractiveness to females was studied in the threespine stickleback (Gasterosteus aculeatus) by presenting dummy or live females to solitary and competing males under different predation risks. In the presence of a predator, males decreased courtship activity. Different courtship components were, however, adjusted to different extents and in opposing directions to predation risk, probably because the single components may have varied in riskiness. The presence of a competing male decreased overall courtship activity, but increased the frequency of zigzags, suggesting zigzagging to be a competitive strategy against other males. In the presence of a predator male courtship activity was not affected by a competitor. Female mate choice correlated with the males' previous frequency of zigzags towards a dummy female. However, when a live female paid attention to a male, the male decreased zigzagging and instead increased leading and fanning behaviours, probably trying to attract the female to the nest to mate. Predation risk affected the attractiveness of males as females reduced their attention to a male when he faced a predator and reduced his courtship activity. As females instead increased their attention to a competing male that had increased his courtship activity, due to decreased competition, males clearly are balancing mating opportunities against predator avoidance. When males vary in their susceptibility to predators, predation risk may thus affect mating success of competing males. Received: 31 January 1997 / Accepted after revision: 15 April 1997     

Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata)

Previous work has shown that under elevated predation risk, male guppies (Poecilia reticulata) switch from courtship to less conspicuous coercive mating attempts. This behavioural transition is traditionally interpreted as a 'risk-sensitive' response that makes males less conspicuous to predators. However, predation risk leads to behavioural changes (such as schooling and predator inspection) in females that may result in coercive mating attempts being more profitable in high-risk situations. Here, we tested the hypothesis that the switch to coercive mating by male guppies in high-risk situations is mediated by adjustments in female behaviour, rather than directly by the predator. We used replicate models resembling a known guppy predator to simulate predation risk in wild-caught guppies from a high-predation population in Trinidad. Our results revealed that males performed proportionately more coercive mating attempts when presented with a female that had been exposed previously to a model predator compared to when males were paired with non-exposed females. Total mating activity (combined rates of courtship and forced mating attempts) did not differ significantly among the two treatment groups, indicating that overall mating activity is unaffected by predation risk. Importantly, when we subsequently presented both sexes concurrently with a predator model, total mating activity and the proportion of forced mating attempts remained unchanged in the high-risk treatment. Taken together, these results indicate that the transition from courtship to forced mating attempts under elevated predation risk is mediated by changes in female behaviour, which we suggest may favour the use of coercive mating under high predation risk.     

Female choice of multiple male criteria in guppies: interacting effects of dominance,coloration and courtship

Summary I experimentally examined the relative importance of social dominance, color patterns, and courtship behavior in male mating and reproductive success in the guppy Poecilia reticulata. Female choice of males is based on a complex set of behavioral and morphological traits. The results of 59 paired-male one-female visual choice and mating trials showed that male mating success was positively correlated with dominance, courtship intensity, and male coloration. Only dominant males engaged in full copoulations, and they sired two-thirds of the broods. An analysis of the paternity of broods and results of mating trials showed that a female's visual response when the sexes are separated by a glass partition is a good predictor of a male's reproductive success when the partition is removed and they are allowed to mate. A canonical correlation analysis of male behavioral and morphological traits indicated that female visual response and male mating success were positively correlated with male courtship and with agonistic behavior. However, the relative importance of color varied. Carotenoid and iridescent spots were important both in attracting the female's attention and in enhancing male mating success. Melanins were not correlated with either mating success or female response. There was a relatively low correlation (48%) between male behavioral and morphological variables and female response variables (full copulation and female visual response). These results suggest that female choice is subtle, and is based on a complex suite of male behavioral and morphological traits as well as on competitive interactions among males.     

Variation in male courtship costs in butterflies

A cost of mating is common to both sexes but has predominantly been examined in females. In species where males provide resources to females at copulation, male mating costs are expected to be high as nutrient provisioning enhancing female fecundity is assumed to carry costs. In addition, males frequently court females prior to mating, which is known to carry survival costs to both sexes. However, the magnitude and basis of variation in males’ mating costs remains largely unknown. Here, I examine the effect of nutrient provisioning and courtship on male longevity across full-sib families in the paternally investing green-veined white butterfly, Pieris napi. Copulating males suffered a survival cost as did courting males prevented from copulating, indicating the courtship component of mating is costly. Male P. napi release aphrodisiacs during courtship to promote mating, indicating that these compounds may also be costly to produce. Contrary to expectation, nutrient provisioning was not associated with reduced survival relative to males only allowed to court females, although it is possible that this could be masked by the potentially elevated courtship rates of courting males relative to mating males. Families differed in magnitude of reduced male survivorship, indicating a likely genetic basis to variation in costs of courtship and copulation. Male weight was unrelated to longevity and mating success, whereas longevity strongly influenced male mating success, indicating lifespan is an important male fitness trait in this species.     

Population and gender-based differences in tissue-specific enzyme activities in brackish water and freshwater threespine sticklebacks, Gasterosteus aculeatus

Sticklebacks (Gasterosteus aculeatus) from a brackish water and a freshwater population were compared immediately after removal from their habitat and after being maintained in the laboratory. Glutamate dehydrogenase activities in the liver and both lactate dehydrogenase and aspartate aminotransferase activities in the axial muscle were higher in the brackish water sticklebacks than in the freshwater specimens. Liver glutamate dehydrogenase activities were higher in males than in females, whereas lactate dehydrogenase activities were distinctly higher in females. A significant positive correlation was found between size and both aspartate aminotransferase and lactate dehydrogenase. The population-specific activities of muscle enzymes are interpreted as an example of evolutionary adaptation of enzyme regulation. Received: 28 February 1997 / Accepted: 5 August 1997     

Sequential female choice and the previous male effect in sticklebacks

Summary Female choice, identified as a major force in sexual selection theory, has recently been demonstrated in a number of species. These tests concentrated on simultaneous choice situations although females have to compare males sequentially in most territorial species, which is the more demanding task. Here it is shown that female three-spined sticklebacks, Gasterosteus aculeatus L., rate sequentially presented males according to their brightness. With increasing costs of sampling the females become less choosy. Furthermore, a male's attractiveness has a significant effect on the female's rating of the next male; a given male is rated higher when preceded by a duller male than by a brighter one and vice versa. Female sticklebacks use a stochastic decision rule in sequential mate choice that is attuned to the attractiveness of the present and previously encountered male. This demonstration of a previous male effect not only indicates an efficient mechanism for finding the best of a number of males but also extends the applicability of sexual selection theory.Offprint requests to: T.C.M. Bakker     

Function of male courtship vocalizations in red-winged blackbirds

Summary During courtship, male red-winged blackbirds (Agelaius phoeniceus) produce long sequences of simple, single-note precopulatory calls, punctuated with occasional songs. Male song has previously been shown to stimulate copulation solicitation in captive, estradiol-implanted females of this species (Searcy and Brenowitz 1988; Searcy, in press). Here I show that sequences of precopulatory calls also stimulate copulation solicitation in female redwings, but that they are not as stimulatory as song. In tests contrasting mixed bouts of song and precopulatory calls with bouts of song alone, the mixed bouts elicited significantly more female solicitation in one instance, more but not significantly more in a second, and an exactly equal amount as song alone in a third. Neither song nor precopulatory calls could be shown to affect proximity of females to the speaker.     

Patterns of courtship behavior and ejaculate characteristics in male red-winged blackbirds

Sperm competition in birds is likely to have important effects on the behavior and physiology of reproduction in both sexes. For males, such competition should select for large sperm reserves and behavioral adjustment of copulation when reserves are low. We investigated both these possibilities in free-living red-winged blackbirds (Agelaius phoeniceus), a highly polygynous species with apparently strong sperm competition. We found that the recent copulatory behavior of males did not affect the propensity to copulate with a model female. Ejaculates collected from individual males at 1-h intervals showed no evidence of sperm depletion, yet repeated ejaculates collected less than 10 min apart did. Male ejaculate size was significantly larger if it was the first one of the day (i.e., after an overnight rest). The average ejaculate size was 12.5 (±12.5 SD) million sperm. Males captured during the breeding season had an average of 111.7 (±52.8) million sperm stored in their seminal glomera. Because males average a peak copulation rate of six per female per day, in one day a male might utilize all the sperm in his seminal glomera if more than two females on his territory are fertilizable. We hypothesize that polygyny and sperm competition in this species have combined to select for rapid replenishment of the seminal glomera throughout the day, in contrast to other species that have been studied. Testis size and sperm reserves of male red-winged blackbirds are intermediate between monogamous species and species with intense sperm competition. Several possible explanations for this are discussed. Received: 21 October 1997 / Accepted after revision: 15 February 1998     

Rhythmic male reproductive behavior controls timing of courtship and mating in Laupala cerasina

In many organisms, mating behavior occurs at a particular time of day, which may be important for avoiding mate competition or interspecific mating. Crickets of the Hawaiian genus Laupala exhibit an unusually protracted courtship in which males produce a series of nuptial gifts prior to the species-typical time of mating. Mating time is one of several rhythmic behaviors that have diverged among closely related Laupala species, which exhibit an extremely high speciation rate. Mating rhythm may reflect direct selection on male and/or female sexual receptivity or the pleiotropic consequence of selection on other rhythmic behaviors. To examine the role of sexual rhythmicity in Laupala cerasina, we characterized the time boundaries or “circadian gate” of courtship and mating, as well as female phonotactic response to male song. We also examined which sex is responsible for mating rhythmicity by phase-shifting males relative to the female photophase. Our results demonstrate that mating behavior is gated by the end of the light phase. Time limits to female mating receptivity were not observed and thus male rhythm alone appears to be responsible for the timing of mating. Furthermore, when courtship is initiated later in the day, males produce fewer nuptial gifts and increase nuptial gift production rate while delaying mating, suggesting that the number of gifts a female receives is important to male reproductive success.     

Effects of male dominance and courtship display on female choice in the ring-necked pheasant

Male traits and behaviours acting in mate choice and intrasexual competition are expected to be congruent. When studying their evolution, this often makes it difficult to differentiate between these two components of sexual selection. Studies are therefore needed on mate choice in conjunction with the role of displays and dominance. We present the results from two experiments conducted to investigate the effects of male dominance and courtship displays on female choice in the ring-necked pheasant, Phasianus colchicus, controlling for differences in morphological male traits. We found: (1) different courtship behaviours had different effects on female choice: females were mainly attracted by the feeding courtship behaviour, while another courtship display (the lateral display) was effective in producing the copulation-acceptance response by the females; (2) subordinate males performed the courtship behaviour before females less frequently than dominant males, and females reinforced intrasexual selection by choosing dominant males, and (3) subordinate males in visual contact with a dominant became less attractive to females. The results support the idea (armament-ornament model) that female pheasants may benefit from using traits selected in male-male competition as clues for mate choice. Received: 23 October 1997 / Accepted after revision: 7 October 1998     

Plasticity in male courtship behaviour as a function of light intensity in guppies

The environment is profoundly important in shaping many aspects of animal phenotype, including courtship and mating behaviours. Courtship displays rely upon the transmission of visual information from the signaller to the receiver, which means they are likely to be less effective in visually poor conditions such as at low light or in turbid ecosystems. One might therefore predict that in visually poor environments it would be beneficial for individuals to plastically adjust their mating behaviour to maximise mating success. Here, we investigate the impact of the developmental and current visual environment (light intensity) upon male mating behaviour in the Trinidadian guppy Poecilia reticulata. Male guppies have two different mating tactics: They can court females with a visual sigmoid display or attempt to circumvent female choice by attempting a non-consensual copulation (gonapodium thrust). We reared juvenile guppies in low light and relatively high light intensities for 5 months before observing individual males for mating behaviour in both light conditions. We found that the current light environment is important in determining the frequency of both sigmoidal courtship displays and non-consensual copulation attempts. Males increase the frequency of sigmoidal displays at relatively high light and increase non-consensual mating attempts at low light, suggesting that males compensate for poor visual conditions via an adjustment in tactics. We also find a significant correlation in courtship effort between the different light environments, suggesting that there is individual consistency across time and context for this trait. Developmental environment was less important. However, we found that fish reared at lower light intensities continued to employ sigmoidal displays despite the poor current visual environment. Our data show that male mating behaviour is phenotypically plastic in response to recent light environment. This may have implications for understanding how animals cope with anthropogenic environmental change.     

Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection

Theoretical and empirical studies suggest that an optimal resistance to pathogens and parasites requires an optimal number of MHC alleles per individual. Here we argue that three-spined sticklebacks (Gasterosteus aculeatus) achieve this goal by applying a strategy that involves a self-referential process. According to this model, females complement their own set of alleles with a more or less diverse set of male alleles such that the combined diversity reaches an optimum. In previous experiments, we have identified allele counting as a major mate-choice strategy in large populations. The self-referential allele-counting hypothesis predicts that MHC-based mate choice favors dissimilar MHC alleles in small populations facing the risk of inbreeding. Therefore, we conducted an experiment that simulated a small effective population size with low MHC class-II diversity. Our experiments are based on the analysis of MHC class-IIB alleles that explain a major part of the overall MHC diversity in sticklebacks, as determined by mathematical modeling. The results show that females preferred males with dissimilar alleles. Our present and the previous studies (which we reanalyzed with respect to our new predictions) show that irrespective of high or low population diversity faced by female sticklebacks for their mate choice, they use information about their own and their potential mate's MHC polymorphism for optimal complementation of their own set of alleles. From combining the data of the previous and the present experiment we found that female sticklebacks try to achieve an optimum number of MHC class-IIB alleles for their offspring through mate choice. The chosen MHC diversity is close to the most frequent diversity found naturally in individual fish, which in addition have the lowest parasite burden.     

On the evolution of nest raiding and male defensive behaviour in sticklebacks (Pisces: Gasterosteidae)

Summary We develop a model to explain the evolution of nest raiding by female sticklebacks based on enhanced female reproductive success derived by creating mating opportunities with the male whose nest has been destroyed. Our model depends critically on the shape of the function relating percentage hatch success to the number of eggs in a male's nest, and the probability that the female will later mate with the male whose nest was raided. Raiding by females will be favoured when the number of eggs in the nest is high providing high egg numbers reduces the percentage hatch rate. High probabilities of mating with the male in question also favour raiding. A second model suggests that males cannot reduce the probability of being raided by limiting the number of eggs in the nest. Instead selection should favour their increasing the number of eggs in the nest. Tests of these models are suggested and their relation to other factors which may influence the evolution of cannibalism are discussed.     

Satellites and sneakers: opportunistic male breeding tactics in pupfish (Cyprinodon pecosensis)

Summary Manipulations of population density, availability of oviposition substrate, and size of breeding habitat affected the proportion of pupfish (Cyprinodon pecosensis) males adopting territorial and satellite breeding tactics. Satellites occupied stations above breeding substrates defended by territorial males. Both territorial and satellite males developed a bright blue breeding coloration. A third breeding tactic, sneak-spawning, was occasionally observed. Sneak-spawning males retained the cryptic female coloration and occasionally spawned on territories. The lower reproductive success of satellites and sneak-spawning males suggested that both are conditional breeding tactics adopted by competitively inferior males. Satellites were present in all treatments that favored a territorial breeding system, but were absent when the breeding system was a dominance hierarchy. Satellites were associated with territorial males that had higher reproductive success and larger territories than males without satellites. Satellites functioned as parasites rather than as mutualists, since they disrupted spawnings and stole copulations from territorial males. The occurrence and frequency of the conditional breeding behaviours in pupfish represent facultative responses of males to changes in the intensity of competition for breeding sites and females.