鱼类亲代抚育行为的研究进展

亲代抚育行为（parental care behavior）是指动物对其后代或其亲缘后代提供保护和养育的所有活动,属于本能行为的一种,广泛存在于动物界之中。鱼类在其为数不多的科中充分发展了几乎所有类型的亲代抚育行为,因而成为研究该行为的最佳物种之一。随着威廉斯原理（Williams’s Principle）的提出和应用,人们对鱼类亲代抚育行为的探索逐步由定性向定量发展,普遍认同了在鱼类进化中,雄性抚育模式得以占据支配地位的缘由并非是因为雄性在抚育活动中获得了较多的利益,而是由于在获取相同利益时雄性损失的未来投资成本较雌性低的观点。近年来的研究证实,在亲代抚育过程中存在着某种动态调整机制,其中四个比较关键的影响因素分别为：亲本所抚育的子代数量、亲本先前的投资、亲本与被抚育子代间的遗传关联度和亲本未来的交配机会。     

Sex differences in parental care: Gametic investment,sexual selection,and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra‐pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male‐biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.     

Devoted fathers or selfish lovers? Conflict between mating effort and parental care in a harem‐defending arachnid

When there is a temporal trade‐off between mating effort and parental care, theoretical models predict that intense sexual selection on males leads to reduced paternal care. Thus, high‐quality males should invest more in mating effort because they have higher chances of acquiring mates, whereas low‐quality males should bias their investment towards parental care. Once paternal care has evolved, offspring value should also influence males’ decisions to invest in offspring attendance. Here, we performed a manipulation under field conditions to investigate the factors that influence male allocation in either mating effort or parental care. We predicted that facultative paternal care in the harem‐holding harvestman Serracutisoma proximum would be negatively influenced by male attractiveness and positively influenced by offspring value. We found that attractive males were less likely to engage in egg attendance and that the higher the perceived paternity, the higher the caring frequency. Finally, egg mortality was not related to caring frequency by males, but predation pressure was much lower than that recorded in previous studies with the same population. Thus, the benefits of facultative male care may be conditional to temporal variation in the intensity of egg predation. In conclusion, males adjust their investment in either territory defence or egg attendance according to their recent mating history and perceived paternity. Our findings suggest that exclusive paternal care can evolve from facultative paternal care only if the trade‐off between mating effort and parental care is circumvented.     

PATERNITY PROTECTION CAN PROVIDE A KICK‐START FOR THE EVOLUTION OF MALE‐ONLY PARENTAL CARE

Sperm competition and uncertainty of paternity hamper the evolution of male parental care. Thus, maternal care predominates in most taxa. What if males can, however, limit cuckoldry by guarding the eggs postmating? Here, we show that this provides a reason to reconsider an old and nowadays rather discredited hypothesis: that external fertilization is associated with male care because the parent who releases its gametes first can depart leaving the other in a “cruel bind,” having to care for the offspring. In our model, protection of paternity provides an additional incentive for the male to stay associated with its young. When we then assume that offspring survive better if guarded, paternity protection proves enough to kick‐start the evolution of male‐only parental care from a scenario with no care. This fits with data from fishes, where male‐only care is associated with external fertilization, whereas female‐only care almost always evolves after an initial transition to internal fertilization. Our model unifies disparate hypotheses regarding parental care roles and provides support for the idea that care roles can be influenced by sex differences in selection to be physically close to the offspring, including selection that is initially not based on offspring survival.     

Sex differences in biparental care as offspring develop: a field study of convict cichlids (<Emphasis Type="Italic">Amatitlania siquia</Emphasis>)

Parental investment theory states that parents should contribute more to older offspring. Differences between the sexes also influence how each parent contributes to offspring in biparental species. Here, we examined a naturally occurring population of biparental convict cichlids in Costa Rica to determine how each parent cared for offspring during two distinct offspring development stages. Consistent with the predictions of the reproductive value hypothesis, we hypothesized that the levels of parental contribution would be relative to the value that each parent places on a brood. We predicted that female parents would contribute more than male parents because female convict cichlids have lower future reproductive success than males. Additionally, we predicted that both parents should contribute more to older offspring, either due to the young’s increased susceptibility to predation (i.e., the vulnerability hypothesis) or because of the longer period of time parents have been interacting with older offspring (i.e., feedback hypotheses). This increase in investment by males should coincide with a change in the coordination of care between parents. Detailed observations of parental pairs in their natural habitat supported these predictions. Females contributed more to broods than males and were relatively unaffected by offspring age while males spent significantly more time with older, free-swimming fry. Additionally, males tended to leave younger offspring more than females did, and were more likely to do so consecutively with younger offspring. This suggests that the coordination of duties between parents changes as parental investment changes. Overall, these data support both the reproductive value and the vulnerability hypotheses, but not necessarily the feedback hypothesis.     

Maternal investment tactics in superb fairy-wrens

In cooperatively breeding species, parents often use helper contributions to offspring care to cut their own costs of investment (i.e. load-lightening). Understanding the process of load-lightening is essential to understanding both the rules governing parental investment and the adaptive value of helping behaviour, but little experimental work has been conducted. Here we report the results of field experiments to determine maternal provisioning rules in cooperatively breeding superb fairy-wrens (Malurus cyaneus). By manipulating carer: offspring ratios, we demonstrate that helpers allow females to reduce the rate at which they provision their brood. Female reductions, however, were less than that provided by helpers, so that chicks still received food at a faster rate in the presence of helpers. Despite this, chicks fed by parents and helpers were not heavier than those provisioned by parents alone. This is because maternal load-lightening not only occurs during the chick provisioning stage, but also at the egg investment stage. Theoretically, complete load-lightening is predicted when parents value themselves more highly than their offspring. We tested this idea by 'presenting' mothers with a 'choice' between reducing their own levels of care and increasing investment in their offspring. We found that mothers preferred to cut their contributions to brood care, just as predicted. Our experiments help to explain why helper effects on offspring success have been difficult to detect in superb fairy-wrens, and suggest that the accuracy with which theoretical predictions of parental provisioning rules are matched in cooperative birds depends on measuring maternal responses to helper presence at both the egg and chick stages.     

Male "mixed" reproductive strategies in biparental species: Trivers was probably right, but why?

Trivers proposed that, if parental care by both sexes is advantageous, males should practice a "mixed" strategy of seeking extrapair copulations, while restricting their parental investment to offspring of social mates. We explore circumstances under which males should limit their parental care in the predicted manner. We find that Trivers's "mixed" strategy will generally be evolutionarily stable so long as either socially monogamous or polygynous males usually sire more offspring per brood from a social mate than they typically sire in broods of extrapair mates. Polygynous males should spread investment across their home nests unless the expected number of chicks sired in them differs widely. Whether polygynous males should restrict paternal care to social mates' offspring hinges additionally on resident male investment in broods containing extrapair young: if resident males contribute minimally, some investment by a polygynous extrapair male becomes more advantageous. Recently reviewed data on extrapair fertilization distributions within monogamous and polygynous passerines suggest that extrapair offspring often predominate numerically within their broods, consistent with sperm expenditure theory. Nevertheless, most species conform to the model's criterion regarding relative parentage levels in broods of social versus extrapair mates. Patterns of extrapair parentage thus appear sufficient to stabilize biparental care systems.     

Female blue tits adjust parental effort to manipulated male UV attractiveness

The differential allocation hypothesis predicts that parents should adjust their current investment in relation to perceived mate attractiveness if this affects offspring fitness. It should be selectively advantageous to risk more of their future reproductive success by investing heavily in current offspring of high reproductive value but to decrease investment if offspring value is low. If the benefits of mate attractiveness are limited to a particular offspring sex we would instead expect relative investment in male versus female offspring to vary with mate attractiveness, referred to as 'differential sex allocation'. We present strong evidence for differential allocation of parental feeding effort in the wild and show an immediate effect on a component of offspring fitness. By experimentally reducing male UV crown coloration, a trait known to indicate attractiveness and viability in wild-breeding blue tits (Parus caeruleus), we show that females, but not males, reduce parental feeding rates and that this reduces the skeletal growth of offspring. However, differential sex allocation does not occur. We conclude that blue tit females use male UV coloration as an indicator of expected offspring fitness and adjust their investment accordingly.     

Geographic variation in the importance of male parental care and mating systems in tree swallows

Sexual selection and mating systems are thought to be influencedby the relative contribution of the sexes toward productionof offspring. Food abundance should influence the value of eachsex's contribution to the production of offspring and, thereby,the level of sexual selection. We examined this hypothesis intwo populations (Alberta and Ontario, Canada) of tree swallows(Tachycineta bicolor) that differed greatly in food abundance.Male removal experiments and natural cases of polygyny indicatedthat females without male parental care produced fewer offspringin the area (Ontario) with less abundant food. Relative to theirmates, males also fed their nestlings more often in Ontariothan in Alberta. Despite the difference between areas in therelative importance of male parental care, we did not find morepolygyny in Alberta than in Ontario. The lack of relationshipbetween frequency of polygyny and the contribution of male parentalcare to offspring production suggests that other factors suchas female-female competition can influence the level of sexualselection independently of sexual differences in parental investment.     

Sex ratio manipulation within broods of house wrens, Troglodytes aedon

Trivers & Willard (1973, Science, 179, 90-92) developed an economic theory of parental investment to explain how the relative profitability of sons and daughters varies under specific ecological conditions. In their maternal condition hypothesis they proposed that in polygynous species, the sex of an offspring should be associated with the amount of parental care likely to be made available to it. In these species, the amount of parental investment directed towards offspring may differentially influence the fitness of male and female offspring because males in better than average condition as adults may enjoy larger fitness gains than a female would if she were in better than average condition, while the reverse may be true when conditions are poor. I tested this hypothesis by determining the sex of specific offspring within house wren broods. Because hatching is asynchronous and fledging is synchronous in this polygynous species, last-hatched young fledge having received less parental care than their broodmates. I predicted that last-hatched offspring would be more likely to be female. I found that these young were indeed more likely to be females, were more likely to have hatched from last-laid eggs and were fledging in poor condition relative to their broodmates. I propose that female house wrens behave in a manner consistent with the predictions of the Trivers & Willard hypothesis by producing female offspring last in the laying sequence of their clutches. Copyright 2000 The Association for the Study of Animal Behaviour.     

Adaptive secondary sex ratio adjustments via sex-specific infanticide in a bird

Infanticide is easiest to understand when it involves killing the offspring of others [1], but a parent may also kill its own offspring if the sacrifice of currently dependent young leads to higher survival of brood mates [2] or an improvement in the parent's likely future reproduction [3]. However, sex-specific infanticide by parents of their own offspring, although occurring in some human societies [4], is rare across species. Its rarity may be because killing one sex combines wasted parental effort with consequent biases in population sex ratios that are detrimental for the fitness of the overproduced sex [5-7]. We show that killing male offspring can be advantageous to Eclectus parrot (Eclectus roratus) mothers even though frequency-dependent selection then elevates the reproductive value of sons above that of daughters. In poorer-quality nest hollows, broods with a single female nestling had higher reproductive value than broods in which the female had a younger brother. Our data demonstrate frequent targeted removal of male nestlings within 3 days of hatching in these specific brood types and nesting conditions. The ability of Eclectus parrots to perceive the sex of their offspring relatively early may favor decisions to kill one sex before further investment in parental care.     

Morphological and genetic predictors of parental care in the North American barn swallow Hirundo rustica erythrogaster

Sexually dimorphic traits often signal the fitness benefits an individual can provide to potential mates. In species with altricial young, these signals may also predict the level of parental care an individual is expected to provide to shared offspring. In this study, we tested three hypotheses that traditionally relate sexually dimorphic traits to parental care in two populations of North American barn swallows Hirundo rustica erythrogaster. The good parent hypothesis predicts a positive relationship between an individual's ornamentation and his or her care whereas the differential allocation (more care given by individuals when paired to high quality mates) and reproductive compensation (more care given by individuals when paired to low quality mates) hypotheses predict that an individual's level of parental investment is relative to the quality of their mate. Male and female North American barn swallows have colorful ventral feathers and elongated tail streamers, but there is evidence that ventral color, not tail streamer length, predicts measures of seasonal reproductive success. Accounting for the positive correlation between within‐pair feeding rates and other potentially confounding variables in all of our models, we found no support for the good parent hypothesis because in both males and females, traits shown to be under sexual selection did not predict feeding rates in either sex. However, our data reveal that male coloration, and not streamer length, predicted a female's provisioning rate to shared offspring (females fed more when paired with darker individuals) in two separate populations, supporting the differential allocation, but not the reproductive compensation hypothesis. Because genetic traits have also been shown to affect parental investment, we evaluated this variable as well and found that a male's paternity did not have significant effects on either male or female feeding rates. Overall, our results suggest that females do not pair with darker males in order to gain direct benefits in terms of his expected levels of parental care to shared offspring, but do themselves invest greater levels of care when paired to darker males. Further, our results are consistent with previous studies which suggest that ventral feather color, not streamer length, is a target of sexual selection in North American populations of barn swallow because females invested more in their offspring when paired to darker mates.     

Can females gain extra paternal investment by mating with multiple males? A game theoretic approach

Although females may require only one mating to become inseminated, many female animals engage in costly mating with multiple males. One potential benefit of polyandrous mating is gaining parental investment from multiple males. We developed two game theoretic models to explore this possibility. Our first model showed that male care of multiple females' offspring evolves when male help substantially increases offspring fitness, future mating opportunity is limited, and group size is small. In our second model, we assumed that males invest in the offspring of former mates and evaluated the fitness consequences of female monogamous and polyandrous mating strategies. Females benefit only from limited polyandry, that is, mating with several males. Polyandry is discouraged because females must share male investment with other polyandrous females, and paternal care is likely to experience diminishing returns. Females may enhance their access to male investment by competing with rival females and monopolizing investment, however. The results support the argument that females can gain paternal investment by mating with several males in small social groups (e.g., dunnocks Prunella modularis). The results do not support the argument that females can gain paternal investment from pronounced multiple mating in large social groups, however, as observed in many primate species.     

Sexual selection determines parental care patterns in cichlid fishes

Despite a massive research effort, our understanding of why, in most vertebrates, males compete for mates and females care for offspring remains incomplete. Two alternative hypotheses have been proposed to explain the direction of causality between parental care and sexual selection. Traditionally, sexual selection has been explained as a consequence of relative parental investment, where the sex investing less will compete for the sex investing more. However, a more recent model suggests that parental care patterns result from sexual selection acting on one sex favoring mating competition and lower parental investment. Using species-level comparative analyses on Tanganyikan cichlid fishes we tested these alternative hypotheses employing a proxy of sexual selection based on mating system, sexual dichromatism, and dimorphism data. First, while controlling for female reproductive investment, we found that species with intense sexual selection were associated with female-only care whereas species with moderate sexual selection were associated with biparental care. Second, using contingency analyses, we found that, contrary to the traditional view, evolutionary changes in parental care type are dependent on the intensity of sexual selection. Hence, our results support the hypothesis that sexual selection determines parental care patterns in Tanganyikan cichlid fishes.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Testosterone and the trade-off between mating and paternal effort in extrapair-mating superb fairy-wrens

High investment in mating and parental effort in male birds are considered mutually exclusive, as testosterone suppresses paternal care and stimulates sexual and aggressive behaviours. Superb fairy-wrens, Malurus cyaneus, are unusual in that males concurrently engage in courtship and paternal care. Fairy-wrens live as stable socially monogamous pairs with up to four subordinate male helpers. The majority of offspring are not sired by any of the males in the group but all group males provide parental care. Throughout the period of care males visit and court neighbouring females. To examine the role of testosterone in this trade-off, I determined the effect of testosterone treatment on the males' time budget, in particular their investment in within- and extrapair sexual behaviours and paternal care. Testosterone did not affect time spent foraging and resting or the number of songs produced. However, the relative investment in sexual and parental behaviours changed, confirming proximate control of this trade-off by testosterone. While there was a large increase in within-pair courtship, which is always rare during the nestling period, testosterone had only a small effect on the most frequent sexual behaviour, extragroup courtship displays. Testosterone failed to induce the maximum frequency of courtship flights of which male fairy-wrens are capable, and I argue that this is because, at prevailing testosterone levels, males are always motivated to leave their territory and social circumstances largely dictate the actual departure rate. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Sex-biased immunity is driven by relative differences in reproductive investment

Sex differences in immunity are often observed, with males generally having a weaker immune system than females. However, recent data in a sex-role-reversed species in which females compete to mate with males suggest that sexually competitive females have a weaker immune response. These findings support the hypothesis that sexual dimorphism in immunity has evolved in response to sex-specific fitness returns of investment in traits such as parental investment and longevity, but the scarcity of data in sex-reversed species prevents us from drawing general conclusions. Using an insect species in which males make a large but variable parental investment in their offspring, we use two indicators of immunocompetence to test the hypothesis that sex-biased immunity is determined by differences in parental investment. We found that when the value of paternal investment was experimentally increased, male immune investment became relatively greater than that of females. Thus, in this system, in which the direction of sexual competition is plastic, the direction of sex-biased immunity is also plastic and appears to track relative parental investment.     

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.     

Models of parent-offspring conflict. II. Promiscuity

The population genetics of Trivers (1974) concept of parent-offspring is examined for species in which the effects of the conflict are felt by future half-sibs, as in promiscuous mating systems in which the male shows no parental care. Whether or not a rare conflictor gene will spread in a non-conflictor population depends on f(m) greater than (m + 1)/(0.5m + 1.5) for a dominant gene, and on f(m) greater than 1/4(7 + 3) for a recessive gene; f(m) is the fitness gained by a conflictor relative to a non-conflictor offspring [f(m) greater than 1], and m is the amount of parental investment taken by a conflictor relative to m = 1 for a non-conflictor. The ESS value for conflict (mo) in promiscuous species with zero male parental care has mo = f(mo)/4[df(mo)/dmo]. However, where the male maintains the same harem for several breeding seasons, or where there is promiscuity but both sexes contribute equally to parental care, conditions for conflict are equivalent to monogamy.     

Energetics of parental care in six syntopic centrarchid fishes

We studied parental behavior in six syntopically breeding species of centrarchid fishes to determine whether energetic costs could contribute to our understanding of the diversity of parental care. We used a combination of underwater videography, radio telemetry and direct observation to examine how the cost of parental care varied with both its duration and intensity. Duration of parental care, activity patterns, and energetic costs varied widely among species. Overall, the duration of care increased with parental size between species. When energetic costs were adjusted for species-specific differences in the duration of parental care, the cost of parental care also increased with mean size of the species. Species with extended parental care exhibited stage-specific patterns of activity and energy expenditure consistent with parental investment theory, whereas fish with short duration parental care tended to maintain high levels of activity throughout the entire period of parental care. The only apparent exception (a species with brief parental care but stage-specific behavior) was a species with multiple breeding bouts, and thus effectively having protracted parental care. These data suggest that some species with short duration parental care can afford not to adjust parental investment over stages of offspring development. Using our empirical data on parental care duration and costs, we reevaluated the relationship between egg size and quality of parental care. Variation in egg size explained almost all of the observed variation in total energetic cost of parental care, and to a lesser degree, duration—the larger the eggs, the more costly the parental care. This research highlights the value of incorporating energetic information into the study of parental care behavior and testing of ecological theory.