No reason to sneak: why males of all sizes can breed in the hole-nesting blenny, Aidablennius sphinx

Most blennioid fishes show a resource-based, promiscuous mating system with alternative 'sneaking' mating tactics. The hole-nesting species, Aidablennius sphinx, however, appears to be an exception; small males did not mimic females, most had their own nest and not once in 20 h of spawning observations did a second male enter a nest. In this field study, we ask if sneaker tactics are constrained and what factors favour independent nesting by small males. Larger males received more eggs sooner and attracted more females than smaller males. Larger males may be preferred because they released more sperm per ejaculation and fanned their eggs more often. In the long-term, however, larger males did not spawn more often than smaller males since: (1) the nests of large males filled up with eggs sooner than the nests of small males; (2) large males refused females more often than small males; and (3) a highly biased ratio of females to preferred large males meant many females had no option but to spawn with small males. Thus, small males nest independently, despite potential for female mimicry tactics (multiple females spawned simultaneously) and simultaneous parasitic spawning (males exited the nest during spawning)     

Paternity and condition affect cannibalistic behavior in nest-tending bluegill sunfish

Theory of parental care evolution predicts that a parent should invest more in a brood when its fitness value is greater than alternative investments such as the parent's own survivorship or future broods. In fish, filial cannibalism (eating one's own offspring) is widespread and represents a challenge to parental care evolution. In this study, I investigated filial cannibalism in bluegill sunfish (Lepomis macrochirus). Bluegill are characterized by alternative mating tactics referred to as "parentals" and "cuckolders". Parentals delay maturation, construct nests, court females and provide sole parental care for the developing offspring. Cuckolders mature precociously and parasitize parentals using two tactics called "sneakers" and "satellites". I found that parentals that obtained fewer eggs during spawning appeared more likely to completely cannibalize their brood (total filial cannibalism: P=0.07), regardless of their condition. Among parentals that provided care, partial cannibalism was greater during the egg phase as compared to the fry phase of care, but it was unrelated to brood size. Throughout the care period, parentals in better condition were less likely to partially cannibalize their brood, indicating that parentals use cannibalism to replenish energy reserves. Independent of condition, parentals that were cuckolded more were more likely to eat part of their brood. This relationship was evident only after the eggs had hatched, which is consistent with data showing that parentals can use olfactory cues produced by fry but not eggs to assess their paternity. This latter result proposes that parentals may be selectively culling cuckolder offspring from their nest. These data provide empirical support for parental care theory, and the first evidence for the importance of paternity on cannibalistic behavior.Communicated by M. Abrahams     

Sperm swimming speed and energetics vary with sperm competition risk in bluegill (<Emphasis Type="Italic">Lepomis macrochirus</Emphasis>)

Under sperm competition, a males fertilization success depends largely on the ejaculate characteristics of competing males. Theoretical models predict that, in external fertilizers, increased risk of sperm competition should result in selection for increased sperm swimming speed. To test this prediction, we studied the behavior of sperm from parental and sneaker male bluegill (Lepomis macrochirus), a fish species characterized by high levels of cuckoldry due to alternative reproductive tactics of males (parentals and cuckolders). Because cuckolders (sneakers and satellites) always spawn in the presence of a parental male, but the reverse is not true, cuckolders experience the greater risk of sperm competition. We show here that the spermatozoa of sneakers have faster initial swimming speeds but shorter periods of motility than the sperm of parental males. Moreover, we show that sperm swimming speeds shortly after activation (when most fertilization occurs) are correlated with starting ATP levels in spermatozoa, suggesting that sperm competition has selected for higher energetic capacity in the sperm of sneakers. Thus, the higher energetic capacity and initial swimming speed of sneaker sperm may explain why, despite having fewer sperm per ejaculate than parentals, sneakers fertilize more eggs than parental males when they compete to fertilize a clutch of eggs.Communicated by L.W. Simmons     

Sperm characteristics associated with different male reproductive tactics in bluegills (Lepomis macrochirus)

We examined the availability and motility of sperm from parental and sneaker male bluegills (Lepomis macrochirus), a colonially nesting sunfish (Family Centrarchidae) with male parental care and a high incidence of cuckoldry by both sneaker and satellite males. We found no differences between sneakers and parentals in length and swimming speed of sperm, or percent and duration of sperm activity. In sneaker milt, however, sperm was almost 50% more concentrated than in parental milt (16.5×10⁶ vs 11.5×10⁶ sperm/μl of milt, respectively). Despite this difference in sperm concentration, stripped ejaculates from sneakers contained almost 400 million fewer sperm (only 32% as many sperm) than those from parentals due to their much smaller stripped ejaculate volumes (only about 19% that of parentals). Thus unless sneakers can compensate by releasing more sperm or gaining closer proximity to eggs at the time of spawning, they may be at a disadvantage with respect to sperm competition. We discuss these results in relation to models for the evolution of alternative reproductive behaviours in this species and suggest that the cuckolders may be making the best of a bad situation. Received: 18 February 2000 / Revised: 23 March 2000 / Accepted: 14 September 2000     

Male–male competition and alternative male mating tactics influence female behavior and fertility in Japanese medaka (Oryzias latipes)

Intense male–male competition driven by high male density during mating can result in the evolution of alternative mating tactics that increase male fertilization success. The effects of alternative male mating tactics on females can range from increased fertilization and genetic benefits to decreased fertilization and loss of paternal care. However, the influence of male competitive behavior and alternative mating tactics on female behavior and reproductive success has seldom been addressed. In this work, I investigated the occurrence of alternative male mating tactics and their potential influence on female behavior and fertilization success in Japanese medaka (Oryzias latipes). Groups of one, two, or four males competed for access to a female in a repeated-measures experiment. Male density had a significant influence on female reproductive output as a result of a change in competitive mode from contest to scramble competition that coincided with more disruption during mating when more than one male attempted to mate. By contrast, sneaking during mating was beneficial to males, as more than one male sired offspring in most spawnings involving sneaker males. These results suggest that there may be conflict between males and females over mating, such that females are detrimentally affected by the occurrence of alternative mating tactics, whereas males may benefit from sneak mating. The occurrence of conflict between the sexes can be related to ecological factors, such as male density, which cause behavioral change in both males and females.     

Sex,food and conflicts: nutrition dependent nuptial feeding and pre-mating struggles in scorpionflies

Female and male reproductive interests often differ. In species in which matings are accompanied by a transfer of resources valuable for both participants, such as nuptial prey gifts, conflicts may readily occur. Scorpionflies may use alternative mating tactics. One is to offer a prey item (dead arthropod) to females in exchange for mating. This prey gift tactic includes a conflict because a male must decide on whether to offer the gift rather than to fight the female and consume the gift. The outcome may depend on the nutritional status of both males and females. Males may be more willing to give if they themselves are satiated and the condition of the females may influence the payoff from the males’ investment. Similarly, females may be more willing to accept food gifts if they are in poor nutritional condition. In this study of the scorpionfly Panorpa cognata, I experimentally manipulated the feeding history of both males and females. I observed the outcome of the direct interactions that followed when males that were holding prey were approached by females. I found that well-fed males offered the food gift sooner than males in poor nutritional condition that fed extensively on the food item before offering. Female condition had no significant influence on whether prey items were offered by males or accepted by females. I also found that well-fed males rarely searched for prey to pursue the prey gift tactic in courtship. Thus, the prey tactic does not seem to be the males’ first option.     

Why do males tolerate sneakers? Tests with the European bitterling, Rhodeus sericeus

In most species, males attack other males that attempt to gain fertilizations through sneak copulations. Here we report on a system where dominant males show a low level of aggression against sneakers at the initial stages of territory establishment. Females of the European bitterling, Rhodeus sericeus, lay their eggs in living mussels and males fertilize the eggs by releasing sperm over the mussels both before and after egg laying. When we allowed males to court females to a mussel containing no eggs at different male densities - one, two, four, or six males - the dominant male showed a low level of aggression against other males that released sperm. The dominant male became aggressive toward the other males only after eggs had been laid. This unusual pattern could be due to either some benefit of accepting sneakers or a high cost of aggression. We found support for both possibilities. The presence of several males decreased the time until a female spawned, whereas increased aggression by the dominant male against other males during a second female presentation, when the male was more territorial, interrupted courtship and increased the time until spawning. Females appeared to be attracted by both the presence of several males around a mussel and increased courtship under male competition. The bitterling mating system possibly differs from that of other species due to lack of investment in nest building and parental care, and high costs of defending the spawning site against sneakers.     

Mating behavior of <Emphasis Type="Italic">Abdopus aculeatus</Emphasis> (d’Orbigny 1834) (Cephalopoda: Octopodidae) in the wild

The mating system of Abdopus aculeatus incorporates sneaker matings, mate guarding, sex-specific body patterns, frequent copulations, and male–male competition for mates, making it more similar to that of aggregating decapod cephalopods than any previously known octopus social system. Large male–female A. aculeatus occupy ‘Adjacent’ (G_A) dens and copulate frequently in mate-guarding situations over successive days. Nearby individuals copulate in ‘Temporary guarding’ (G_T) and ‘Transient’ (T; non-guarding) situations, the latter of which can involve ‘Sneaker’ (S) mating. In a focal animal study of these octopuses in the wild (Sulawesi, Indonesia) we addressed the hypotheses that they demonstrate: (1) precopulatory mate choice, (2) differential copulation rates by individuals employing different mating tactics, and (3) distant sex identification. We quantified daily copulation rates of A. aculeatus of reproductive size as well as aspects of copulation duration, display, mate-competition, and mate rejection. Mating tactic correlated with daily copulation rates. ♂G_A spent significantly more time copulating than did ♂T, while ♀G_A spent more than twice as much time per day in copula than did other females. Sneaker copulations lasted longer than those by males adopting other tactics. Mate-guarding was an effective and important tactic used by males to temporarily monopolize mating with apparently non-selective females. Males demonstrated clear pre-copulatory mate choice by guarding and mating repeatedly with large females (typically ♀G_A). While foraging alone away from the den, ♂G procured ‘Transient’ copulations with unguarded females. However, mate-guarding reduced the amount of time ♂G were alone and may impede their ability to seek out new mates. Low-copulation rates by ♀T, the smallest female tactic on average, may reflect this trade-off between mate preference and mate-searching by males, or non-receptivity of some females. A male-typical body pattern (black and white stripes) appeared to facilitate distant sex identification. Although mating and aggression were often initiated before contact between individuals, same-sex copulations and intense male–female aggression were rare. By contrast frequent male–female copulations and intense male–male aggression were consistent behavioral components of mating in A. aculeatus at these sites. Because the behavioral and ecological characters conducive to this complex system are not exclusive to A. aculeatus, it is possible that other octopuses exhibit some or all of these behaviors. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Sperm competition risk affects male mate choice copying

Mate choice copying was mostly described as a strategy employed by females to assess the quality of potential mates, but also males can copy other males’ mate choice. An open question in this context is whether and how copying males evaluate sperm competition risk, as mating with a female that has already copulated with another male obviously sets the stage for intense sperm competition (i.e., in species with internal fertilization). Using the livebearing Atlantic molly (Poecilia mexicana) as a model, we asked (a) whether males of that species indeed copy other males’ choices, and if they do so, (b) whether copying males strategically adjust their behavior to sperm competition risk. We used an approach where focal males could first choose to associate with a large or a small stimulus female. Mate choice tests were then repeated after an “observation phase” during which either no model male was present (treatment 1, control) or the previously non-preferred female could be seen associating (treatment 2) or physically interacting (treatment 3) with a model male. We found that, after the observation phase, males spent considerably more time with the previously non-preferred female in treatment (2), i.e., they copied the model male’s choice. This effect was much weaker during treatment (3) where sexual interactions between the model male and the formerly non-preferred female were allowed. Males, therefore, seem to adjust their copying behavior strategically to the perceived risk of sperm competition.     

Mating effort and female receptivity: how do male guppies decide when to invest in sex?

Males vary in the degree to which they invest in mating. Several factors can explain this variation, including differences in males’ individual condition and the fact that males allocate their energy depending on the context they face in each mating attempt. Particularly, female quality affects male reproductive success. Here, we studied whether male guppies (Poecilia reticulata) strategically allocated more mating effort, in terms of mating behaviour and male–male competition, when they were matched with a receptive (R) female than a non-receptive one. In accordance with our prediction, we found that males increased their mating behaviour when they were with a receptive female. Even though male guppies can inseminate non-receptive females, we only found high levels of courtship between males that were with a receptive female rather than a non-receptive one. Although there was little affect of female receptivity on male–male competition, we found that males chased and interrupted courtships more with receptive females than with non-receptive females regardless of odour. Finally, we also studied whether the sexual pheromone produced by receptive female guppies is a cue that males use in order to increase their mating effort. We found that males were more attracted to a female when they perceived the sexual pheromone, but only increased their mating and aggressive behaviours when females showed receptive behaviour. This strategic increase in mating effort could result in higher male reproductive success because mating attempts towards receptive females are likely to be less costly and males could have a greater probability of fertilisation.     

Solitary nesting as an alternative breeding tactic in colonial nesting bluegill sunfish (Lepomis macrochirus)

Colonial breeding can evolve in response to benefits afforded by clumped individuals, such as reduced predation and increased ease of assessing potential mates. However, colonial breeding can also impose costs such as increased disease transmission or increased cuckoldry. Here, we investigate solitary nesting as a potential alternative breeding tactic in colonial breeding bluegill sunfish (Lepomis macrochirus). Most male bluegill, termed parentals, compete for nesting sites in colonies and then court and spawn with females and provide sole care of the eggs. Although nesting in a colony results in reduced predation and fungal infection of broods, it comes at a cost of increased parasitism by specialized cuckolder males that do not nest. We found that 4.5% of parentals forgo spawning in a colony and instead construct nests solitarily. Solitary males were of similar size and age to colonial males, but were in significantly better condition. Solitary males obtained as many eggs as males nesting in the center of colonies, and significantly more than males nesting on the periphery of colonies. Thus, females do not appear to discriminate against solitary males. Solitary males had smaller ear tabs, a presumed sexually selected character used by parental males in intrasexual competition, than colonial males. Tracking data revealed consistency in nesting tactic (but not nest position within the colony) between spawning attempts. We suggest that solitary nesting represents either a facultative decision made by parental males in top condition at the onset of breeding, or a life history decision to forgo spawning in colonies.Communicated by K. Lindström     

Female spawning patterns and male mating success in the sand goby Pomatoschistus minutus

In June 1989 in a study conducted near Träminne Zoological Station, Finland (60° N 23° E) I investigated whether or not male mating success could be explained by female choice for male size in sand gobies (Pomatoschistus minutus). Male mating success was constrained by nest size and increased markedly with increasing nest size. I also found a negative correlation between the length of spawning females and the fullness of the nest. As large females lay more eggs, they also need to find a nest with more space available for the eggs. The size of males without eggs was the same across nest size, whereas the size of males with eggs significantly increased with increasing nest size. This is interpreted as female discrimination against males as mates in nests that are often contested. There was no correlation between a male's size and his mating success when males with no eggs in their nests were excluded. A male removal experiment, however, showed that, in a specific nest, when male size increases so does mating success, whereas, if male size decreases, mating success also decreases. It is concluded that in the sand goby females prefer to mate with larger males, especially when the male possesses a high-quality nest that he most probably will have to defend against other males.     

Male-male interference competition decreases spawning rate in the European bitterling (<Emphasis Type="Italic">Rhodeus sericeus</Emphasis>)

We investigated the consequences of male-male interference competition associated with alternative male mating tactics in a freshwater fish, the European bitterling (Rhodeus sericeus). Male bitterling defend territories around living mussels and attract females to lay their eggs in the gill cavities of mussels. We experimentally manipulated spawning-site abundance and male density at two spatial scales. We showed that the total number of eggs spawned by females was constrained by the number of mussels available for oviposition. The effect was mediated by behavioral interactions among competing males because of variation in the Operational Sex Ratio (OSR) in close proximity to a mussel and not by a direct limitation in mussel capacity to accommodate the eggs. Both total and local male densities affected spawning behavior, and interacted in their effect on female spawning rate. Territorial male aggression caused courtship interruptions that prolonged the time until successful spawning and increased with male density. However, territoriality broke down at the highest male density, with a consequent stabilizing effect on spawning rate.Communicated by J. Krause     

Alternative mating tactics in the Italian treefrog, <Emphasis Type="Italic">Hyla intermedia</Emphasis>

As in many lekking anurans, Italian treefrog males use two mating tactics: they can attract females by calling vigorously or be satellites, that is, they can remain silent in proximity of a calling male and try to intercept females attracted by their neighbour. We investigated the factors that affected the expression of this mating tactic. Consistent with the conditional mating tactic hypothesis, satellites were smaller than average and smaller than their parasitised calling males. They spent a larger-than-average number of nights at the breeding site, where most of them were also observed calling. Moreover, satellites showed lower call rates and lower mating success than those of males they parasitise but not lower than those of males they did not parasitise. Overall, these results, together with those derived from the analyses of the seasonal and spatial distribution of males, provide evidence for a non-random association between satellites and calling males and are consistent with the hypothesis that satellites have spectral and temporal acoustic preferences that parallel those of females. By adopting the less-successful satellite mating tactic, competitively inferior males can nevertheless maximise their potential reproductive fitness by sexually parasitising the most attractive chorusing 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.     

Sequential polyandry affords post-mating sexual selection in the mouths of cichlid females

Females mating with multiple males may obtain direct benefits such as nuptial gifts or paternal care or indirect (i.e. genetic) benefits resulting in higher-quality offspring. While direct benefits are easily identified, it is difficult to determine indirect benefits, and it is hence largely unclear how they are obtained. This is particularly true in species with external fertilisation, where females seem to have little control over fertilisation. In cichlids, most maternal mouthbrooders show sequential multiple mating, where females visit several males for egg deposition. Genetic data revealed that multiple paternity of eggs and young in the mouth of females is common, but behavioural data of female spawning decisions are missing. Here, we test four hypotheses to explain female multiple mating in the maternally mouthbrooding cichlid, Ophthalmotilapia ventralis: (1) fertilisation insurance, (2) genetic bet-hedging, (3) female choice and (4) ‘sperm shopping’ (i.e. induction of sperm competition resulting in sexually selected sperm). Detailed observations of spawning behaviour in the field combined with histological analyses of the male reproductive organs suggest that fertilisation insurance, genetic bet-hedging and pre-mating female choice are unlikely to explain the sequential female multiple mating in O. ventralis. Instead, cryptic female choice by sperm shopping, i.e. post-mating sexual selection, is most compatible with our data and might be the major ultimate cause of multiple mating in females of this species and of mouthbrooding cichlids with maternal care in general. Our study provides new insight into ultimate causes of sequential polyandry in species with external fertilisation, as hitherto post-mating sexual selection by cryptic female choice has been assumed to be incompatible with external fertilisation mechanisms except by components of the ovarian fluid.     

Factors predicting male fertilization success in an external fertilizer

In postcopulatory sexual selection both sperm competition and cryptic female choice are considered to be important selective agents, but their relative importance for male fertilization success has received little attention. We tested whether sperm quality, male spawning coloration, male heterozygosity, and genetic overlap with the female explained a male’s fertilization success in controlled in vitro fertilization competition trials between equal numbers of sperm from pairs of male Arctic charr (Salvelinus alpinus), an external fertilizer. Offspring were genotyped to determine each males’ share of paternity. The velocity of a male’s sperm relative to the velocity of the competing male’s sperm was the best predictor of male fertilization success. Yet, sperm velocity was not related to spawning coloration or male heterozygosity. In fact, the most brightly colored male in a pair had the lowest fertilization probability. This could result from cryptic female choice for pale males, but might rather be a result of paler males producing more competitive sperm than more colored males. Furthermore, the more microsatellite alleles a male shared with the female relative to the competing male, the higher fertilization success he had. We argue that this latter may be an effect of assortative cryptic female choice, which might prevent hybridization with sympatric Arctic charr morphs or one form of kin selection.     

Evolution of mating systems and sexual size dimorphism in North American cyprinids

Mating systems evolve with sexual size dimorphism (SSD) in many animals. Mating systems with males larger than females occur when males compete for female access or guard territories, while mating systems with group mating tend to occur in species where females are the same size or larger than males. In addition to variation in SSD with mating system, sperm competition varies among mating systems in predictable patterns. We examined the evolution of mating systems with SSD and testes mass in 111 North American Cyprinidae fishes using phylogenetic comparative methods. Our results demonstrate that the evolution of mating systems in Cyprinidae fishes is from ancestral taxa that are group spawners with females the same size or larger than males to pair spawning systems where males tend to be larger than females. We used an additive model to predict male and female body size from testes mass and mating system. Only mating system varied predictably with SSD. Our results for analyses of hyperallometry (Rensch’s rule) were that individual species of Cyprinidae can have hyperallometry for SSD, but the pattern is not present across all taxa.     

Independent effects of male and female density on sexual harassment, female fitness, and male competition for mates in the western mosquitofish Gambusia affinis

Operational sex ratio (the ratio of sexually active males to fertilizable females) has a major influence on male competition for mates and male–female interactions. The contributions of male and female density per se to mating system dynamics, however, are rarely examined, and the fitness consequences are often inferred rather than quantified. Male mosquitofish (Gambusia affinis) compete aggressively and frequently harass females for copulations, a behavior thought to reduce female fitness. Female fitness can also be reduced by increases in female density, which may affect food availability, cannibalism rates, and chemical interactions between females. I manipulated male and female densities of G. affinis to measure their effects on male–male aggression, male harassment toward females, and female fitness. I found that males chased rivals more often and attempted fewer copulations when female density decreased, but surprisingly male density had no significant effect on the frequency of these male behaviors. In contrast, males’ agonistic displays toward other males increased with male density, but display behavior was unaffected by female density. These results suggest that male and female density do not always contribute equally or at all to the patterns of behavior we observe. Female fitness declined as female density increased, the opposite pattern expected if male harassment is costly to females. This suggests that a strong, negative effect of female density overwhelmed any potential costs of male harassment. Sources of female density dependence and the consequences of changes in male and female density to patterns of male behavior are discussed.     

O brother,where art thou? The varying influence of older siblings in rank acquisition by female baboons

Males in sexually dimorphic species like baboons appear to have surprisingly little influence on the reproduction and dominance ranks of their female kin, even though they could potentially increase their fitness by helping their relatives improve their ranks. Male baboons are able to dominate females several years before they emigrate, but their presence has no effect on relatives’ dominance ranks, at least when female kin are present. As a result, females usually acquire ranks within their matriline, above their older sisters. We describe the process of rank acquisition among orphaned and non-orphaned juvenile and adolescent females in a group of free-ranging baboons. Orphaned females were significantly more likely than non-orphaned females to acquire unexpected ranks. Orphaned females with older sisters often acquired ranks within the matriline, but below their older sisters’. Orphaned females with older brothers were likely to rise in rank above their matriline. Females’ interventions on behalf of younger sisters always supported the existing female dominance hierarchy, while males’ interventions tended to act against it. Similarly, in playback experiments, females appeared to be willing to support their younger sister only in disputes with lower-ranking females. In contrast, males appeared to be willing to support their sister even in disputes with higher-ranking females. Fraternal support enables females to improve their dominance ranks, but only if their mothers have died. It remains a puzzle why males have so little influence on their female relatives’ ranks when female kin are present, and so much when they are absent.