Brood mixing and reduced polyandry in a maternally mouthbrooding cichlid with elevated among-breeder relatedness

Uniparental maternal brood care often coincides with multiple paternity and single maternity of broods, possibly reflecting benefits of polyandry and costs of uniparental care. Genetic data from the maternally mouthbrooding cichlid fish Simochromis pleurospilus revealed the opposite pattern--low polyandry and allomaternal care. More than 70% of the investigated females had mated with a single male, and 14% of the females had unrelated fry in their broods. Broods with foreign fry were in the late stage of brood care, in which females guard free-swimming fry and recall the broods into their mouths for protection. With one exception, fostering females were related to their adopted fry at the level of first cousins (R(QG) > 0.12), but relatedness between fosters and adopted fry was not significantly higher than between fosters and fry tended by other females. Relatedness among breeders extended to the level of first-order relatives. Mean relatedness among contemporaneously breeding dams (R(QG) = 0.08) was significantly higher than among dams breeding in different seasons (R(QG) = -0.04), which suggests a temporal or spatial concentration of mouthbrooding relatives. Indeed, females sometimes brood in small groups. This behaviour may reduce brood predation but will increase the risk of brood mixing, which is possibly mitigated by low costs of brood care and indirect benefits accrued by relatedness among the breeders in the group. Remarkably, the apparent inbreeding potential did not give rise to bet-hedging polyandry or active avoidance of relatives, as half of the mated individuals were related at R(QG) > 0.13 and polyandry did not coincide with high within-pair relatedness.     

Host-parasite kinship in a female-philopatric bird population: evidence from relatedness trend analysis

Conspecific brood parasitism (CBP), an alternative reproductive tactic where some females lay eggs in the nests of other females of the same species, occurs in many animals with egg care. It is particularly common in waterfowl, for reasons that are debated. Many waterfowl females nest near their birthplace, making it likely that some local females are relatives. We analyse brood parasitism in a Hudson Bay population of common eiders, testing predictions from two alternative hypotheses on the role of relatedness in CBP. Some models predict host-parasite relatedness, others predict that parasites avoid close relatives as hosts. To distinguish between the alternatives, we use a novel approach, where the relatedness of host-parasite pairs is tested against the spatial population trend in pairwise relatedness. We estimate parasitism, nest take-over and relatedness with protein fingerprinting and bandsharing analysis of egg albumen, nondestructively sampled from each new egg in the nest throughout the laying period. The results refute the hypothesis that parasites avoid laying eggs in the nests of related hosts, and corroborate the alternative of host-parasite relatedness. With an estimated r of 0.12-0.14, females laying eggs in the same nest are on average closer kin than nesting neighbour females. Absence of a population trend in female pairwise relatedness vs. distance implies that host-parasite relatedness is not only an effect of strong natal philopatry: some additional form of kin bias is also involved.     

Male reproductive skew, paternal relatedness, and female social relationships

Female social relationships among primates are thought to be shaped by socio-ecological factors and phylogenetic constraints. We suggest that patterns of paternal relatedness among females influence measures of social tolerance that have been used to classify species into different social relationship categories. As kin support and kin preference have only been measured for matrilineal kin and related individuals exchange less aggression and have a higher conciliatory tendency, the observed low nepotism levels and high tolerance levels may be an artifact of hidden paternal relatedness among the nonkin category. Using comparative data on macaques, we investigate this hypothesis using male reproductive skew as a proxy for paternal relatedness. Within the limitations of the study we show that populations classified as being less nepotistic, and more tolerant exhibit higher levels of reproductive skew. This first result and the reasoning behind may motivate future students of social relationships to take paternal relatedness into consideration. Potential implications of this finding if repeated with larger samples include that variation in aspects of macaque social relationships may be explained without considering phylogeny or the strength of between-group contest competition for food.     

Brood parasitism by cowbirds: risks and effects on reproductive success and survival in indigo buntings

We observed brood parasitism by brown-beaded cowbirds (Molothrusater) on indigo buntings (Passerina cyanea) and estimated dieimpact of parasitism on the success of the individual buntingsin their current nests and in their future survival and reproduction.Rates of parasitism over 8 years were 26.6% in 1040 nests and19.8% in 693 nests in two areas in southern Michigan. Risk ofparasitism was high early in the season; half the bunting nestswere begun after the end of the cowbird season. Risk was independentof female age, plant containing the nest, or habitat The immediatecost of parasitism was 1.19 and 1.26 fewer buntings fledgedper nest. Bunting success was lower in parasitized nests withcowbird eggs (nests were more likely to be deserted or predated),lower when the cowbird nestling failed (nests were more likelyto be predated), and lower when the cowbird fledged (fewer buntingsfledged) compared to nonparasitized nests. Costs were due toremoval of a bunting egg when die cowbird laid its own egg andto competition for parental care of the cowbird and buntingnestlings. Buntings that fledged from nests where a cowbirdalso fledged were only 18% as likely to survive and return totheir natal area in the next year as buntings from nests wherea cowbird did not fledge. Long-term effects of cowbird parasitismon adult breeding later in the season, survival to the nextseason, and reproductive success in the next season were negligiblewhen compared between birds that reared a cowbird and birdsthat reared only a bunting brood, or between birds that wereparasitized and birds that escaped parasitism. The results indicatelittle long-term cost of brood parasitism on individual fitnessof adult buntings beyond the impact on the current nest andthe survival of buntings that fledge from it; nearly all costis to the parasitized brood.     

Host-parasite relatedness in wood ducks: patterns of kinship and parasite success

We investigated the role of kinship in intraspecific nest parasitismof wood ducks (Aix sponsa). Among waterfowl, female philopatrycreates the potential for female relatives to nest in proximity.Costs of intraspecific nest parasitism to host females may bereduced if parasites lay eggs with kin. However, previous observationsof marked wood ducks indicated that females avoided parasitizingclutch mates or the female that incubated them. To further examinethe role of kinship, we determined the genotypes of 27 host-parasitepairs at five microsatellite loci. Average relatedness betweenhosts and all females laying parasitic eggs was only 0.04 ±0.03. Parasites appeared to choose hosts randomly with respectto kinship from among females with nests in the neighborhoodand those within the entire study area. However, host relatednessto the parasite with the greatest number of young leaving thenest was 0.11 ± 0.03, which was greater than expectedif eggs were accepted randomly from neighboring females or fromfemales present on the entire study area (p = .03 and p = .02,respectively). These patterns may reflect parasitism of randomlyselected nests followed by differential acceptance by hosts,differential hatching success of related parasites (e.g., dueto greater laying synchrony), or a mixture of parasitic strategies,one with a focus on related hosts and the other on unrelatedhosts. Genetic data revealed that social relationships did notalways reflect true relatedness and that success of primaryparasites was associated with kinship to hosts.     

Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns

Successful Polistes dominulus nests can be started by one ormore nest founding queens (foundresses). Consequently, thereis much interest in the specific benefits that induce cooperationamong foundresses. Here, we experimentally demonstrate one majorbenefit of cooperation, namely that multiple foundresses increasecolony productivity. This increase is close to the value predictedby subtracting the productivity of undisturbed single-foundresscolonies from the productivity of undisturbed multiple-foundresscolonies. However, we found no evidence that an associatingfoundress' contribution to colony growth is preserved if shedisappears (assured fitness returns). Our correlational datasuggest that cooperation provides survival benefits, multiple-foundresscolonies are more likely to survive to produce offspring thanare single-foundress colonies, and individual foundresses inmultiple-foundress groups are less likely to disappear beforeworker emergence than foundresses nesting alone. Therefore,association provides substantial productivity and survival benefitsfor cooperating foundresses.     

Alternative tactics and individual reproductive success in natural associations of the burying beetle, Nicrophorus vespilloides

Alternative reproductive tactics can be maintained through differentevolutionary avenues. They can be genetically or stochasticallydetermined, in which case they must yield equal fitness, ortheir use can be conditional, in which case the fitness payoffof alternatives may differ. We attempted to assess the reproductivesuccess of alternative reproductive tactics employed by wildmale and female burying beetles in natural associations on carcassesplaced in the field. A beetle's reproductive tactic was definedby its potential involvement in care of larvae, and parentagewas assessed using oligolocus DNA fingerprinting of offspringand potential parents. Both in males and in females, alternativetactics yielded significantly different reproductive benefits:subordinate females (brood parasites) and males (satellite males)had considerably lower reproductive success than dominant oruncontested individuals. Joint breeding was too infrequent forstatistical inferences, generating intermediate offspring numbers.About 15% of offspring were sired by males not present on thecarcass, suggesting that mating away from reproductive resourcescan produce reproductive benefits to males. Our results, inconcert with the observation that beetles using one tactic canbe manipulated into employing the alternative, support the notionthat Nicrophorus vespilloides uses alternatives conditionally,opportunistically employing lower-benefit tactics when moreprofitable tactics are not available, or as additional "on-the-side"tactics to bolster reproductive success.     

Differential responses to related hosts by nesting and non-nesting parasites in a brood-parasitic duck

Host-parasite relatedness may facilitate the evolution of conspecific brood parasitism, but empirical support for this contention remains inconclusive. One reason for this disparity may relate to the diversity of parasitic tactics, a key distinguishing feature being whether the parasite has a nest of her own. Previous work suggests that parasites without nests of their own may be of inferior phenotypic quality, but because of difficulties in identifying these parasitic individuals, little is known about their host selection criteria. We used high-resolution molecular maternity tests to assign parasitic offspring to known parasites with and without their own nests in a population of Barrow's goldeneyes (Bucephala islandica). We determined whether parasite nesting status, host-parasite relatedness and distance between host and parasite nests affected the probability of parasitizing a host and the number of eggs laid per host. We also investigated whether nesting parasites, conventionally nesting females and non-nesting parasites differed regarding their age, structural size, body condition, nesting phenology or total brood size. The probability of engaging in parasitism increased with host-parasite relatedness and spatial proximity to host nests for nesting and non-nesting females alike. However, nesting parasites increased the number of eggs donated with relatedness to the host, while non-nesting parasites did not do so. Non-nesting parasites laid fewer eggs in total, but did not differ by any of the other quality measures from conventional nesters or nesting parasites. Our study provides the first demonstration that nesting and non-nesting parasites from the same population may use different host selection criteria.     

Steroid hormones in bluegill, a species with male alternative reproductive tactics including female mimicry

The proximate mechanisms underlying the evolution and maintenance of within-sex variation in mating behaviour are still poorly understood. Species characterized by alternative reproductive tactics provide ideal opportunities to investigate such mechanisms. Bluegill (Lepomis macrochirus) are noteworthy in this regard because they exhibit two distinct cuckolder (parasitic) morphs (called sneaker and satellite) in addition to the parental males that court females. Here we confirm previous findings that spawning cuckolder and parental males have significantly different levels of testosterone and 11-ketotestosterone. We also report, for the first time, that oestradiol and cortisol levels are higher in cuckolders than in parental males. The two cuckolder morphs did not differ in average levels of any of the four hormones. However, among satellite males which mimic females in appearance and behaviour, there was a strong negative relationship between oestradiol levels and body length, a surrogate for age. This finding suggests that for satellite males, oestradiol dependency of mating behaviour decreases with increasing mating experience. Although such decreased hormone dependence of mating behaviour has been reported in other taxa, our data represent the first suggestion of the relationship in fishes.     

Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika

Telmatochromis vittatus (Cichlidae) is a Tanganyikan substrate brooder which spawns in the gastropod-shell nests of a cichlid, Lamprologus callipterus. We describe male reproductive tactics of T. vittatus in and around the shell nests, where males of various sizes were found. Based on utilization patterns of the shell nests, interactions among males, and spawning behaviors, males could be categorized into four types based on reproductive tactics and in order of body size: sneaker males, satellite males, territorial males and piracy males. Size range of males in tactic groups rarely overlapped. Territorial males defended shell nests harboring multiple females, but during pair-spawning they were occasionally taken over by large piracy males that visited several nests repeatedly. Small sneaker males darted to pair-spawning territorial males and might ejaculate sperm. Satellite males did not perform parasitic spawning but pair-spawned in a single shell outside the nests. Spawning of satellite males was infrequently parasitized. The largest gonado-somatic index (GSI) was found in sneaker males followed by piracy males, territorial males and satellite males, suggesting that gonadal investment of males using the four tactics may be consistent with intensity or risk of sperm competition.     

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth‐brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth‐brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth‐brooding cichlids is discussed.     

Coevolution of female fidelity and male help in populations with alternative reproductive tactics

In socially monogamous species, pair-bonded males often continue to provide care to all offspring in their nests despite some degree of paternity loss due to female extra-pair copulation. Previous theoretical models suggested that females can use their within-pair offspring as ‘hostages'' to blackmail their social mates, so that they continue to provide care to the brood at low levels of cuckoldry. These models, however, rely on the assumption of sufficiently accurate male detection of cuckoldry and the reduction of parental effort in case of suspicion. Therefore, they cannot explain the abundant cases where cuckolded males continue to provide extensive care to the brood. Here we use an analytical population genetics model and an individual-based simulation model to explore the coevolution of female fidelity and male help in populations with two genetically determined alternative reproductive tactics (ARTs): sneakers that achieve paternity solely via extra-pair copulations and bourgeois that form a mating pair and spend some efforts in brood care. We show that when the efficiency of mate guarding is intermediate, the bourgeois males can evolve to ‘specialize'' in providing care by spending more than 90% of time in helping their females while guarding them as much as possible, despite frequent cuckoldry by the sneakers. We also show that when sneakers have tactic-specific adaptations and thus are more competitive than the bourgeois in gaining extra-pair fertilizations, the frequency of sneakers and the degrees of female fidelity and male help can fluctuate in evolutionary cycles. Our theoretical predictions highlight the need for further empirical tests in species with ARTs.     

Resource availability,mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics

The expression of alternative reproductive tactics can be plastic and occur simultaneously depending on cues that vary spatially or temporally. For example, variation in resources and sexual selection intensity is expected to influence the pay‐off of each tactic and shape the decision of which tactic to employ. Males of the nuptial gift‐giving spider Pisaura mirabilis can adopt three tactics: offering a genuine prey gift, a ‘worthless’ non‐nutritious gift or no gift. We hypothesized that resources and/or male body condition, and mating opportunity and sexual selection intensity, vary over the course of the mating season to shape the co‐existence of alternative traits. We measured these variables in the field over two seasons, to investigate the predictions that as the mating season progresses, (i) males become more likely to employ a gift‐giving tactic, and (ii) the likelihood of switching from worthless to genuine gifts increases. Prey availability increased over the season and co‐varied with the propensity of males to employ the gift‐giving tactic, but we found no support for condition‐dependent gift giving. Males responded to an increase in female availability by increasing their mating effort (gift production). Furthermore, the frequency of genuine gift use increased with sexual selection intensity, consistent with the assumption that sperm competition intensity increases with time. Our results suggest that the frequency of alternative tactics is shaped by seasonal changes in ecological factors and sexual selection. This leads to relaxed selection for the gift‐giving tactic early in the season when females are less choosy and resources more scarce, and increased selection for genuine gifts later in the season driven by mating opportunity and risk of sperm competition.     

Impact of male alternative reproductive tactics on female costs of sexual conflict under variation in operational sex ratio and population density

Sexual conflict over mating rate is both pervasive and evolutionarily costly. For females, the lifetime reproductive fitness costs that arise through interactions with potential mates will be influenced by the frequency of such interactions, and the fitness cost of each interaction. Both of these factors are likely to be influenced by variation in operational sex ratio (OSR) and population density. Variation in OSR‐ and density‐dependent male alternative reproductive tactics (ARTs) may be particularly important if the fitness costs that females experience vary with the reproductive tactics that males express. Using a simple model, we consider several examples of OSR‐ and/or density‐dependent variation in male ARTs and the frequency of male–female interactions, and find that variation in the expression of male ARTs has the potential to augment or diminish the costs of frequent male interactions for females. Accurately documenting variation in the expression of male ARTs and associated female fitness costs will benefit future work in this area.     

Social semantics: toward a genuine pluralism in the study of social behaviour

Pluralism is the coexistence of equivalent theoretical frameworks, either because they are historically entrenched or because they achieve separate insights by viewing the same process in different ways. A recent article by West et al. [Journal of Evolutionary Biology (2007) vol. 20, 415-432] attempts to classify the many equivalent frameworks that have been developed to study the evolution of social behaviour. This article addresses shortcomings in the West et al.'s article, especially with respect to multilevel selection, in a common effort to maximize the benefits of pluralism while minimizing the semantic costs.     

Alternative reproductive tactics in male eastern gray squirrels: "making the best of a bad job"

Male eastern gray squirrels (Sciurus carolinensis) congregatearound and pursue a female on her single day of estrus. Thetactics of uniquely marked adult males were monitored duringwinter mating bouts from 1986 to 1990 to examine variation inmale copulatory success. Two tactics were chosen by males: activepursuit or satellite. Active-pursuit males were dominant anddefended proximity to females. Satellite males were subordinateand remained dispersed in the female's home range. Active pursuitwas used only by males 2.75 years old. The switch point betweenthe tactics is about 3 years. Copulations were not distributedevenly among males, with about 30% of all adult males failingto copulate during a breeding season. Active pursuit was themost successful strategy, with male success attributed to theability to defend access to the female. However, satellite malessuccessfully copulated due to the escape of females from dominantmales. Females appear to avoid the overt aggression characteristicof the competition among active-pursuit males by running fromthe group of males. Male success after a female's breakawaywas evenly distributed between the two tactics and accountedfor all copulations by satellite males. The activepursuit andsatellite tactics appear to be a conditional evolutionarilystable strategy where young, subordinate males are "making thebest of a bad job".     

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour,sperm characteristics and social interactions

While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free‐living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down‐regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite‐directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.