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。     

Parental care: a freshwater phenomenon?

Synopsis Attempts have been made to explain the over-representation of parental care in teleost fish families in freshwater habitats by selection due to environmental conditions typical of freshwater. I argue that alternative hypotheses, such as selection for pelagic spawning in marine habitats, can account for the pattern. The fact that parental care is less common among primary freshwater fishes contradicts the view that there is strong selection for parental care in fresh waters, and suggests that phylogenetic relationships must be taken into account.     

Fishes as models in studies of sexual selection and parental care

Fishes are by far the most diverse group of vertebrates. This fact is in no way, however, reflected in their use as model organisms for understanding sexual selection or parental care. Why is this so? Is it because fishes are actually poor models? The usefulness of fishes as models for sexual selection and parental care is discussed by emphasizing some problems inherent in fish studies, along with a number of reasons why fishes are indeed excellently suited. The pros and cons of fishes as models are discussed mainly by comparison with birds, the most popular model organisms in animal behaviour. Difficulties include a lack of background knowledge for many species, and the problems of marking and observing fishes in their natural environment. Positive attributes include the diversity of lifestyles among fishes, and the ease with which they can be studied experimentally in the laboratory. How useful fish models can be is briefly illustrated by the impressive and broadly relevant advances derived from studies of guppies Poecilia reticulata and three‐spined sticklebacks Gasterosteus aculeatus . A selection of topics is highlighted where fish studies have either advanced or could greatly enhance, the understanding of processes fundamental to animal reproductive dynamics. Such topics include sex role dynamics, the evolution of female ornamentation and mate choice copying. Finally, a number of potential pitfalls in the future use of fish as models for sexual selection and parental care are discussed. Researchers interested in these issues are recommended to make much more extensive use of fish models, but also to adopt a wider range of models among fishes.     

Where are all the moms? External fertilization predicts the rise of male parental care in bony fishes

Parental care shows remarkable variation across the animal kingdom, but while maternal and biparental care are common in terrestrial organisms, male‐only care dominates in aquatic species that provide care. Using the most complete phylogenetic tree of bony fishes to date, we test whether the opportunity for external fertilization in aquatic environments can explain the more frequent evolution of male care in this group. We show that paternal care has evolved at least 30 times independently in fish and is found exclusively in externally fertilizing species. Male care is positively associated with pair spawning, suggesting that confidence in paternity is an important determinant of the evolution of care. Crucially, while female care is constrained by other forms of reproductive investment, male care occurs more frequently when females invest heavily in gamete production. Our results suggest that moving control of fertilization outside of the female reproductive tract raises male confidence in parentage and increases the potential for paternal care, highlighting that in an aquatic environment in which fertilization is external, paternal care is an effective reproductive strategy.     

The adaptive significance of parental role division and sexual size dimorphism in breeding shorebirds

Sexual size dimorphism among 57 species in the shorebird family Scolopacidae is evaluated in relation to parental role division during breeding. Normal size dimorphism, i.e. the female being smaller than the male, occurs in species where the female has the main responsibility for parental care, whereas reverse size dimorphism, the most common pattern among shorebirds, is associated with reversed parental roles. Pronounced dimorphism between sexes occurs, besides in body size, also in bill length, where the sex undertaking the main part of brood attendance has a disproportionately short bill in species adapted for foraging by deep probing. A small body size is of adaptive value to attain high parental efficiency for energetic reasons, because smaller individuals need less energy to maintain themselves. Short bills may be advantageous during brood attendance when feeding mainly takes place in terrestrial habitats together with the chicks. Females released from parental care duties are favoured by a larger body size allowing increased accumulation of energy reserves for egg production. There are obvious parallels between shorebirds and raptors concerning the adaptive significance of reverse sexual size dimorphism and parental role division.     

Parental Fin Digging by Cichlasoma octofasciatum (Teleostei: Cichlidae) and the Effect of Parents' Satiation State on Brood Provisioning

Although parental care in fishes does not usually include provisioning offspring after hatching, various types of brood provisioning have been documented for some bony fishes, and in particular, for cichlids. For example, fin digging occurs among biparental substrate brooding cichlids of the ‘genus’ Cichlasoma sensu lato. Parental fin digging by Cichlasoma octofasciatum was investigated under laboratory conditions. Fin digging was performed significantly more often by females than by males. For both sexes, the frequency of fin digging increased significantly with brood age, especially from ages 3 to 10 d of fry: this was more pronounced in females. The parents' own current satiation state during performance of fin digging influenced the fin digging frequency: for both sexes it was higher in hungry than in satiated parents.     

Patterns of multiple paternity and maternity in fishes

The characterization of patterns of multiple mating is a major facet of molecular ecology and is paramount to understanding the evolution of behaviours associated with parental care and mate choice. Over the last 15 years, fishes have been particularly well studied with respect to multiple maternity and paternity thanks to the widespread application of microsatellite markers. The present review focusses on the impressive literature on genetic parentage in fishes. In studies of natural populations, we find that multiple paternity is extremely common across fish species, whereas rates of multiple maternity are much more variable. In species with nest defence, for example, rates of multiple maternity are strongly bimodal, and the occurrence of multiple dams per brood is either rare or the rule. The sex of the care‐giving parent is correlated with the rate of multiple parentage: when males provide uniparental care, rates of multiple paternity are low compared to rates of multiple maternity; when females provide parental care, either alone or assisted by males, rates of multiple paternity are highly variable, whereas rates of multiple maternity are quite low. These patterns may reflect conflicts between the reproductive interests of males and females. We also find that fishes in which females brood the offspring internally display much higher rates of multiple paternity compared to mammals or birds, whereas reptiles are intermediate. Male‐nesting fish species, however, show rates of multiple paternity more similar to those found in other vertebrates. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 735–760.     

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.     

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.     

Life history evolution in cichlids 1: revisiting the evolution of life histories in relation to parental care

Empirical links between egg size and duration of parental care in fishes have generated a considerable amount of theory concerning life history evolution. However, to date, this link has not been investigated in relation to other important life-history traits such as clutch size and body size, or while controlling for shared ancestry between species. We provide the first phylogenetically based tests using a database with information on egg size, clutch size, body size and care duration in cichlid fishes (Cichlidae). Multiple regression analyses, based on independent contrasts on both the species and the genus level, showed that clutch size is the variable most closely related to duration of care. This pattern appeared to be driven by post-hatch care relationships. Our results show that, contrary to expectation, there is no positive link between egg size and care duration in Cichlidae. Instead, greater reproductive output through increased clutch size investment appears to have coevolved with greater care of offspring. We suggest that re-evaluation of the generality of current models of the evolution of egg size under parental care in fishes is needed.     

Do egg size and parental care coevolve in fishes?

A phenomenon that has attracted a substantial theoretical and empirical interest is the positive relationship between egg size and the extent of parental care in fishes. Interestingly, despite the effort put into solving the causality behind this relationship over the past two decades it remains largely unsolved. Moreover, how general the positive relationship between egg size and parental care is among fishes is also poorly understood. In order to stimulate research exploring egg size and parental care variation in fishes, the potential selective forces from both natural and sexual selection on egg size and parental care are discussed. Recent empirical findings on how oxygen requirements and developmental times may differ between differently sized eggs are incorporated into a critical view of the current theory of this field. Furthermore, it is suggested that the up to now neglected effects of sexual selection, through both mate choice and sexual conflict, can have strong effects on the relationship between egg size and parental care in fishes. In light of the recent developments of comparative and experimental methods, future approaches that may improve the understanding of the relationship between egg size and care in fishes are suggested.     

Paternity and paternal effort in the pumpkinseed sunfish

Theoretical models suggest that males should adjust their parentaleffort according to paternity when parental effort is costly,paternity varies among clutches, and males have a cue to assesspaternity. To date, nearly all tests of this theory have beenconducted using birds as model organisms. In this study we examinedthese three factors and the relationship between paternity andmale parental care in a fish system. In the pumpkinseed sunfish(Lepomis gibbosus), parental care is provided exclusively bymales (parentals), but some males (sneakers) parasitize othersby sneaking fertilizations. Parental males significantly lostweight during the parental care period. Clutch size and amountof parental effort did not affect a male's probability of obtainingmore eggs. Paternity was variable among broods. The proportionof young sired by a parental male was not associated with frequencyof fanning eggs or defense of hatched young, but was positivelycorrelated with levels of nest defense during the egg stage.Egg survivorship might restrict an adjustment of fanning behavior,and a general decline in parental behavior (with brood age)might explain the lack of adjustment once the eggs hatch. Parentalmales did not adjust their care when we experimentally manipulatedone possible cue of paternity. Together, these results indicatethat male pumpkinseeds do adjust their care in relation to paternity,but the cues used to assess paternity are not clear.     

Diverse parentage relationships in paternal mouthbrooding fishes

While mouthbrooding is not an uncommon parental care strategy in fishes, paternal mouthbrooding only occurs in eight fish families and is little studied. The high cost of paternal mouthbrooding to the male implies a low risk of investment in another male''s offspring but genetic parentage patterns are poorly known for paternal mouthbrooders. Here, we used single-nucleotide polymorphism genetic data to investigate parentage relationships of broods of two mouthbrooders of northern Australian rivers, mouth almighty Glossamia aprion and blue catfish Neoarius graeffei. For N. graeffei, we found that the parentage pattern was largely monogamous with the brooder male as the sire. For G. aprion, the parentage pattern was more heterogeneous including observations of monogamous broods with the brooder male as the sire (73%), polygyny (13%), cuckoldry (6%) and a brood genetically unrelated to the brooder male (6%). Findings demonstrate the potential for complex interrelationships of male care, paternity confidence and mating behaviour in mouthbrooding fishes.     

The Relationship of Spawning Mode to Conservation of North American Minnows (Cyprinidae)

Approximately 20% of North American minnows are considered imperiled. The factors responsible for imperilment in this group are complex, but the relationship of spawning mode to conservation of North American minnows has not been explored. I provide a summary of the spawning modes of imperiled North American minnows, discuss patterns between these modes and conservation status, and predict the spawning modes for several poorly-known imperiled species. Of the 46 species of North American minnows that are imperiled, spawning modes are known for only 13 species. All spawning modes are represented in the imperiled group of minnows except mound-building and egg-clustering, and with the exception of crevice-spawners and pit-ridge-builders, the percentage of imperiled minnows in each category of spawning mode is roughly proportional to the percentage of minnows in that category overall. Species with complex spawning modes, such as mound-building, pit-building and egg-clustering, are among the most common fishes in North American streams. This pattern suggests that there is a relationship between parental care and success (lack of imperilment) in minnows. Spawning mode is an important consideration in the formulation of recovery plans and proactive conservation efforts.     

Genome size reduction in the chicken has involved massive loss of ancestral protein-coding genes

Both mean genomes size and the variance in genome size among species are smaller on average in birds (class Aves) than in the other tetrapod classes. In order to test whether loss of protein-coding genes has contributed to genome size reduction in birds, we compared the chicken genome and five mammalian genomes. Numbers of members (paralogs) were significantly lower in the chicken gene families than in the corresponding mammalian families. Phylogenetic analyses of chicken, mammal, and fish paralogs supported the hypothesis that chicken-specific loss of paralogs occurred much more frequently than mammal-specific gene duplications. Moreover, the phylogenetic analyses supported the hypothesis that a substantial majority of the paralogs lost in chicken originated from duplications prior to the most recent common ancestor of tetrapods and bony fishes. In addition to loss of paralogs, numerous gene families present in the mammalian genomes were missing in the chicken genome; over 1,000 of these families were found in bony fishes, implying presence of the family in the tetrapod ancestor. In the set of families with more members on average in the mammals than in the chicken, immune system function was associated with a greater degree of gene family size reduction in the chicken, consistent with other evidence that immune system gene families have become particularly compact in birds.     

Phylogenetic perspectives in the evolution of parental care in ray-finned fishes

Among major vertebrate groups, ray-finned fishes (Actinopterygii) collectively display a nearly unrivaled diversity of parental care activities. This fact, coupled with a growing body of phylogenetic data for Actinopterygii, makes these fishes a logical model system for analyzing the evolutionary histories of alternative parental care modes and associated reproductive behaviors. From an extensive literature review, we constructed a supertree for ray-finned fishes and used its phylogenetic topology to investigate the evolution of several key reproductive states including type of parental care (maternal, paternal, or biparental), internal versus external fertilization, internal versus external gestation, nest construction behavior, and presence versus absence of sexual dichromatism (as an indicator of sexual selection). Using a comparative phylogenetic approach, we critically evaluate several hypotheses regarding evolutionary pathways toward parental care. Results from maximum parsimony reconstructions indicate that all forms of parental care, including paternal, biparental, and maternal (both external and internal to the female reproductive tract) have arisen repeatedly and independently during ray-finned fish evolution. The most common evolutionary transitions were from external fertilization directly to paternal care and from external fertilization to maternal care via the intermediate step of internal fertilization. We also used maximum likelihood phylogenetic methods to test for statistical correlations and contingencies in the evolution of pairs of reproductive traits. Sexual dichromatism and nest construction proved to be positively correlated with the evolution of male parental care in species with external fertilization. Sexual dichromatism was also positively correlated with female-internal fertilization and gestation. No clear indication emerged that female-only care or biparental care were evolutionary outgrowths of male-only care, or that biparental care has been a common evolutionary stepping stone between paternal and maternal care. Results are discussed in the context of prior thought about the evolution of alternative parental care modes in vertebrates.     

The Evolution of Male and Female Parental Care in Fishes

In this paper we propose an explanation for (a) the predominanceof male care in fishes, and (b) the phylogenies and transitionsthat occur among care states. We also provide a general evolutionarymodel for studying the conditions under which parental careevolves. Our conclusions are as follows: (i) Parental care hasonly one benefit, the increased survivorship of young. It may,however, have three costs: a "mating cost," an "adult survivorshipcost," and a "future fertility cost." (ii) On average, malesand females will derive the same benefit from care. They probablyalso pay the same adult survivorship cost. However, their matingcost and future fertility costs may differ, (iii) A mating costusually applies only to males. However, this cost may be reducedby male territoriality and, in some situations, be entirelyremoved. Under this condition, natural selection on presentreproductive success is equivalent for males and females, (iv)When fecundity accelerates with body size in females, whilemale mating success follows a linear relationship with bodysize, future fertility costs of parental care are greater forfemales than males. Although further tests are needed, a preliminaryanalysis suggests this often may be the case in fishes. Thus,the predominance of male parental care in fishes is not explainedby males deriving greater benefits from care, but by males payingsmaller future costs. Males thus accrue a greater net fitnessadvantage from parental care (see expressions [6] and [12]).(v) The evolution of biparental care from uniparental male caremay occur because male care selects for larger egg sizes andincreased embryo investment by females. This increases the benefitto the female of parental care, (vi) By contrast, uniparentalfemale care may originate from biparental care when males areselected to desert. This occurs when female care creates a matingcost to males. In some cases male desertion may "lock" femalesinto uniparental care. However, in many other cases femalesmay be selected to desert, giving rise to "no care." (vii) Theorigin of uniparental female care from no care is rare in externallyfertilizing fishes. This is because the benefits of care rarelyoutweigh a female's future fertility costs (expression [9]).For internally fertilizing species, however, the benefit ofcare is high whereas the cost is probably low. Most of thesespecies have evolved embryo retention, (viii) When parentalcare begins with male care and moves to biparental care, ouranalysis suggests that care evolution will include cyclicaldynamics. Parental care in some fishes may thus be seen as transitionaland changing through evolutionary time rather than as an evolutionarilystable state. In theory, "no care" may be a phylogeneticallyadvanced state.     

Sex differences in life history drive evolutionary transitions among maternal,paternal, and bi‐parental care

Evolutionary transitions among maternal, paternal, and bi‐parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life‐history characteristics (stage‐specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi‐parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi‐parental, bi‐parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex‐specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi‐parental → paternal, maternal → bi‐parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life‐history differences between the sexes can drive evolutionary transitions among different sex‐specific patterns of care. The finding that simple life‐history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter‐sexual life‐history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.     

Androgen and behavior in the male three-spined stickleback,Gasterosteus aculeatus. II. Castration and 11-ketoandrostenedione effects on courtship and parental care during the nesting cycle

Courtship declines and ceases while parental care increases in the presence of developing eggs during the nesting cycle of the male three-spined stickleback, Gasterosteus aculeatus. Furthermore, circulating 11-ketotestosterone (11KT) levels are higher during the initial "courtship phase" than during the later "parental phase," similar to that found in other paternal fishes. This study aimed to investigate a possible functional relationship between changes in 11KT levels and changes in reproductive behavior during the nesting cycle. To this end, groups of nonspawned and spawned male sticklebacks were sham-operated, castrated, or castrated and treated with 11-ketoandrostenedione (11KA), and the effects of the treatments on courtship and parental care were studied. Castration removed circulating 11KT, while 11KA replacement prevented the natural decline in 11KT during the parental phase (11KA converts to 11KT extratesticularly), as assessed by radioimmunoassay. Regardless of treatment, parental care remained low and courtship was present in all nonspawned males, even at the end of the experiment. However, courtship did eventually decline in castrated nonspawned males compared to the other two nonspawned groups. In all treatments of spawned males there was a drastic decline in courtship and an increase in parental care. In castrated spawned males, however, the decline in courtship came earlier than in the other two spawned groups. 11KA treatment did not prevent the natural decline in courtship/increase in parental care in spawned males, indicating that the natural decline in 11KT is not responsible for the main portion of the rapid changes in these behaviors over the stickleback's nesting cycle. The limited effects of castration also exclude other gonadal hormones from being responsible for most of these changes.