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.     

雌性选择与雄鸟鸣唱的进化

鸣唱是许多鸟类的重要的雄性第二性征之一。雄性鸣唱包含着丰富的信息：物种、领域质量、遗传状态和生理状态。这些信息可被雌性用来判断潜在配偶的素质,而雌性对复杂鸣唱的偏爱反过塑造了鸟类的鸣唱。一般认为雌性选择的调控基因位于决定性别的W染色体上。     

Interspecific Differences in the Response of Female Birds to Song Repertoires

The functional significance of the wide variation between bird species in the sizes of individual song repertoires is not understood. We have studied the effects of song repertoires on females. Song triggers copulation solicitation display in female sparrows treated with estradiol. Song sparrow males (Melospiza melodia) have repertoires of about 10 song types, and female song sparrows display significantly more to presentations of large repertoires than to a single song type. By contrast, male field sparrows (Spizella pusilla) and white-throated sparrows (Zonotrichia albicollis) each have only one song type, and their females show no significant increment in responsiveness to repertoires of several song types over a single song type. Swamp sparrows (Melospiza georgiana) fall in between, with male repertoires of three song types. Female swamp sparrows behave in intermediate fashion, responding more to several song types than to one, but the response increment is less than in song sparrows. Thus species differences that males exhibit in song repertoires are paralleled by differences in female responsiveness to multiple song types, implicating variations in female reactivity in the evolution of song repertoires. Female song sparrows respond preferentially to repertoires programmed in eventual variety rather than immediate variety, while field sparrows and white-throated sparrows show no discrimination.     

Parental Care: The Key to Understanding Endothermy and Other Convergent Features in Birds and Mammals

Birds and mammals share a number of features that are remarkably similar but that have evolved independently. One of these characters, endothermy, has been suggested to have played a cardinal role in avian and mammalian evolution. I hypothesize that it is parental care, rather than endothermy, that is the key to understanding the amazing convergence between mammals and birds. Endothermy may have arisen as a consequence of selection for parental care because endothermy enables a parent to control incubation temperature. The remarkable ability of many birds and mammals to sustain vigorous exercise may also have arisen as a consequence of selection for parental care because provisioning of offspring often requires sustained vigorous exercise. Because extensive parental care encompasses a wide range of behaviors, morphology, and physiology, it may be a key innovation that accounts for the majority of convergent avian and mammalian characters.     

The Allure of the Distinctive: Reduced Sexual Responsiveness of Female Guppies to 'Redundant' Male Colour Patterns

Frequency-dependent mating behaviour has the potential to maintain genetic variation in characteristics of organisms. The colour patterns of guppies ( Poecilia reticulata ) provide an example of one of the most extreme genetically based polymorphisms known in nature, for which frequency-dependent mate choice could be a mechanism. Numerous studies have shown that female guppies base mating preferences on male colour patterns and there is evidence that females prefer to mate with males displaying novel or unfamiliar colour patterns. This preference could lead to frequency-dependent mating success in males. Nevertheless, the possibility that female sexual responsiveness itself may depend on the frequency of male types has not been tested systematically in guppies or any other species. This study examined the sexual responses of female guppies in experimental groups consisting of two males with similar (redundant) and two males with different (unique) colour patterns. We found that female guppies were much more likely to respond sexually to the displays of unique males than to those of redundant males. Further, there was no effect of orange colouration on female responsiveness as has been documented for this population in several previous studies, thus, discrimination against redundant male types appears to have overridden directional selection based on colour pattern characteristics. This discrimination against redundant male types could in turn lead to frequency-dependent mating success in males and maintenance of colour pattern polymorphism.     

Impacts of Tree Rows on Grassland Birds and Potential Nest Predators: A Removal Experiment

Globally, grasslands and the wildlife that inhabit them are widely imperiled. Encroachment by shrubs and trees has widely impacted grasslands in the past 150 years. In North America, most grassland birds avoid nesting near woody vegetation. Because woody vegetation fragments grasslands and potential nest predator diversity and abundance is often greater along wooded edge and grassland transitions, we measured the impacts of removing rows of trees and shrubs that intersected grasslands on potential nest predators and the three most abundant grassland bird species (Henslow’s sparrow [Ammodramus henslowii], Eastern meadowlark [Sturnella magna], and bobolink [Dolichonyx oryzivorus]) at sites in Wisconsin, U.S.A. We monitored 3 control and 3 treatment sites, for 1 yr prior to and 3 yr after tree row removal at the treatment sites. Grassland bird densities increased (2–4 times for bobolink and Henslow’s sparrow) and nesting densities increased (all 3 species) in the removal areas compared to control areas. After removals, Henslow’s sparrows nested within ≤50 m of the treatment area, where they did not occur when tree rows were present. Most dramatically, activity by woodland-associated predators nearly ceased (nine-fold decrease for raccoon [Procyon lotor]) at the removals and grassland predators increased (up to 27 times activity for thirteen-lined ground squirrel [Ictidomys tridecemlineatus]). Nest success did not increase, likely reflecting the increase in grassland predators. However, more nests were attempted by all 3 species (175 versus 116) and the number of successful nests for bobolinks and Henslow’s sparrows increased. Because of gains in habitat, increased use by birds, greater production of young, and the effective removal of woodland-associated predators, tree row removal, where appropriate based on the predator community, can be a beneficial management action for conserving grassland birds and improving fragmented and degraded grassland ecosystems.     

Reproductive Signals of Female Lizards: Pattern of Trait Expression and Male Response

Relative to the volume of studies concerning the function and evolution of male‐biased sexually dimorphic traits, instances of female‐biased sexual dimorphisms remain largely unstudied, especially in species with conventional sex roles. I investigated the signal function of a female‐specific ornamental trait using the striped plateau lizard (Sceloporus virgatus, Phrynosomatidae) as a model system. During the reproductive season, female S. virgatus develop orange color on their throats that is absent in conspecific males. I established the relationship between color expression and female reproductive state, and determined male response to female color. I show that dynamic changes occurring within the color patch can potentially identify each stage of the female reproductive cycle, largely because of a lag in patch growth relative to color intensification. Sexual receptivity is associated with intense patches rapidly growing in size; ovulation occurs near peak color expression; and the unreceptive period is associated with large patches fading in intensity. Because females express orange color during both the receptive and unreceptive periods, the pattern of color expression is consistent with the courtship‐stimulation and courtship‐rejection hypotheses of signal function. Males may preferentially associate with females that have more highly developed color patches during the courtship season, and/or ignore such females when they are unreceptive. An examination of male behavior towards unfamiliar females indicates that female color has a role in courtship stimulation but has little, if any, role in courtship rejection. During the pre‐mating season, males maintained significantly closer affiliation with, and tended to perform more social behavior towards females with more intense color. During the post‐mating season, female color had no apparent effect on male behavior. The evolution and current function of female ornaments may vary among taxonomically‐related species as a result of differences in ecology, social system, and life‐history.     

Sex Allocation in Response to Maternal Condition: Different Tactics of Care-Giving by Male and Female Zebra Finches

While behavioral ecologists have studied sex allocation for 30 yr, almost nothing is known about the roles of male vs. female parents in making secondary allocation decisions in species with bi‐parental care. To investigate possible sex differences in tactics in zebra finches, we manipulated the condition of one cohort of females by trimming their flight feathers; a second cohort of females and all males were left intact. Focal observations of feeding behavior revealed that manipulated females did not reduce their feeding time, but rather focused their efforts on rearing sons, while control females allocated effort to rearing daughters. Males mated to manipulated females tended to focus effort to daughters, while control males showed no consistent response. Manipulated females experienced a lower reproductive rate, primarily because of a low daughter rate, relative to control females. Manipulated females also laid smaller clutches and had longer inter‐clutch intervals, which suggest that their ability to metabolize and allocate essential proteins from pectoral muscle mass during the egg‐laying period was impaired. To our knowledge, this study is the first to show that parents of both sexes make active sex allocation decisions when the physiological condition of one parent is manipulated; males do not simply adopt female allocation patterns, but make complementary adjustments. Our results have implications for interpretation of handicapping studies that seek to understand the dynamics of inter‐sexual negotiations of care‐giving. Investigation of sex differences in sex allocation tactics in species with limited dietary protein, such as granivorous birds, is a potentially important direction for future research.     

Seasonal Variation in Female Response to Male Calling Song in the Field Cricket, Gryllus rubens

Conspicuous traits that make males attractive to females may make them vulnerable to predators. Females that approach conspicuous males may increase their risk of predation. This means that selection for reduced male conspicuousness in the presence of predators may be due to sexual selection resulting from altered female behavior in the face of increased predator risk. We examine this hypothesis in the field cricket, Gryllus rubens, in which male calling song attracts both conspecific females for mating and parasitoid flies (Ormia ochracea) which kill their hosts within a week. Female crickets are also parasitized by these flies as a result of associating with calling males. In northern Florida crickets that emerge in the spring are not subject to fly parasitism whereas autumn crickets encounter large numbers of flies. We predicted that autumn females should be less attracted to male song than spring females. We tested female response to male calls in a rectangular arena in which male calling song was broadcast from a speaker. Spring females readily approached the speaker but autumn females were less likely to approach and remain in the vicinity of the speaker. These results emphasize the importance of considering how risk affects the evolution of conspicuous male behavior both directly through its effect on the male and indirectly through its effect on female responses to males.     

Male and Female Parental Roles in the Monogamous Cichlid, Tilapia mariae, Introduced in Florida

We documented male and female parental roles of a monogamous fish, the spotted tilapia, Tilapia mariae, in channelized rivers in southern Florida, where this species dominated the fish fauna within 10 years of their introduction. Clearly differentiated parental roles existed between males and females, with females performing nearly all tending of embryos and most tending of free embryos. After young became free-swimming and left the nest, however, males took over primary tending of the school of young while the female patrolled the perimeter of the school and performed nearly all chases directed at predators. Male and female T. mariae also traded off vigilance and feeding, and showed a high degree of intrapair coordination. Experimental removal of one or both parents had major effects on parental behavior and brood survival and integrity. Solitary females took on a parental role intermediate between that of the male and female of a pair. Untended broods were attacked by predators and scattered into aquatic vegetation, and were not observed to reform. Under dense nesting conditions we observed adoption of broods, group rearing of free-swimming young and the presence of non-breeder satellites sharing and defending a territory with breeders. This highly complex parental care may have allowed T. mariae to invade fish communities dominated by uniparental centrarchids, as well as allowing them to use disturbed habitats such as channelized rivers that are of poor quality for nesting and rearing offspring.     

Parental Investment and Territorial/Sexual Behavior in Male and Female Reed Warblers: Are they Mutually Exclusive?

The behavioral and endocrine changes from prenesting to feeding phases of reproduction were examined in free-living reed warblers. Apart from the onset of feeding behavior, these changes in males are particularly evident in song, territorial behavior and circulating levels of testosterone. The interactions between an individual's physiology and behavior during these behavioral transitions were tested first by correlating song and feeding rates with circulating levels of testosterone and secondly by implanting feeding males with steroids and documenting the resulting effects on song, territoriality and parental behavior. The physiological mechanisms associated with the transition from the sexual phase (nest-building and egg-laying) to the parental (incubation and feeding) in females were also examined. In this case, estrogens were implanted during the parental phase to enhance sexual behavior. The results demonstrate an antagonistic relationship between sexual/territorial behavior and parental care in males which is mediated by changes in circulating androgens and no such antagonism in females. The effects of parental manipulation on the feeding rates of the partners and the growth rates of offspring have been examined to shed light on the necessity for male parental input.     

Environmental Effects on Male Reproductive Success and Parental Care in the Florida Flagfish Jordanella floridae

Models of optimal parental care predict that parental investment should depend on offspring value or the effect parental care has on offspring benefits. Few studies have examined the effect of external factors that influence offspring survival and the cost of care. In this study on the Florida flagfish (Jordanella floridae), a species with male parental care, we examined whether environmentally induced changes in care result from changes in egg requirements or in parental costs. We manipulated salinity and temperature, as these factors are known to affect the metabolic rate in both eggs and parents. We predicted that if the change in care behavior is determined by costs to the male then it should be paralleled by changes in non‐egg‐directed behavior. Conversely, if egg‐directed behavior changes independently of other behavior it would suggest that behavior is determined primarily by egg requirements. In addition we examined patterns of mating success under the assumption that if male care is affected by environmental factors then female preferences may change accordingly. Males decreased egg‐directed behavior (fanning and cleaning of eggs) at high salinity. Non‐egg‐directed behavior was unaffected by salinity. Temperature had no effects on behavior. Thus, we conclude that changes in egg demands are primarily responsible for the observed results. Successful males were bigger and more aggressive. This suggests that male dominance was an important determinant of male mating success. Unsuccessful males showed significantly more variation in number of red stripes with respect to salinity than successful males. Unsuccessful males may be less able to regulate color expression under varying environmental conditions, in which case color may be an indicator of male quality. We replicated the experiment early and late in the season. Males did not change their effort in care over the season. However, care (fanning) in the absence of eggs increased towards the end of the season. Since pre‐mating fanning was positively correlated to a male’s eventual mating success we conclude that males increased their effort to attract mates late in the season.     

A Test for Male Parental Care in a Fundulid, the Bluefin Killifish, Lucania goodei

Under field conditions, breeding male bluefin killifish, Lucania goodei, have been observed aggressively defending territories from other breeding males, non-breeding females, and minnows (mainly Notropis harperi). We performed an aquarium experiment to test whether male aggression serves to protect newly deposited eggs from predation. We allowed a male and a female to spawn in a yarn mop, removed the female, and exposed the eggs to one of four treatments (spawning male present, two minnows present, spawning mal+two minnows present, no adult fish present). Mops were censused daily for seven days. Egg predation rates were highest in the male+minnows and male only treatments. Egg predation rates in the male+minnows treatment did not differ from the predicted predation rate (sum of male only and minnows only treatments). Hence, there is no evidence for male parental care in L. goodei. In addition, we compared the egg predation rates (filial cannibalism) between males of 3 different color morphs and found no evidence for differential egg cannibalism.     

Effects of Exogenous Testosterone on Parental Care Behaviours in Male Bluegill Sunfish (Lepomis macrochirus)

Androgens are known to mediate aggressive and defensive behaviour in many vertebrate species. However, high concentrations of androgens might also conflict with the expression of nurturing behaviours and therefore a trade‐off can exist between aggressive and nurturing behaviours during parental care. We explored the role of testosterone in paternal care in bluegill sunfish (Lepomis macrochirus), where males provide both sole defence of the young from predators and sole nurturing behaviour such as fanning of the eggs. At the onset of parental care, we manipulated testosterone levels in males using testosterone propionate implants. We then observed the frequency of nurturing and aggressive behaviours displayed by the males over 6 d of parental care. Testosterone‐implanted fish were more aggressive when presented with a brood predator, performing more bites, opercular flares and lateral displays than control males. Testosterone‐implanted males, however, were not less nurturing than control fish, performing similar levels of fanning and nest‐cleaning behaviours. Thus, our results support a positive relationship between testosterone and paternal aggression but no testosterone‐mediated trade‐off between paternal nurturing and aggression.     

Variable Parental Care in a Labrid Fish: How Care Might Evolve

Hypotheses for the evolution of parental care suggest several intermediate stages between no care and full care. To shed light on how care might evolve, I describe intermediate stages within one species. These include spawning behavior ranging from out-of-nest spawning, (which involves no parental care) to algal nests and associated male parental care (plus intermediate stages between the two previous categories), all observed in the same individual males of the peacock wrasse, Symphodus tinca. About 20% of males go through transitional stages from no care to full care as the season progresses. These stages are: 1) following females over large areas, 2) focusing on an area about 10 × 10 m, 3) chasing other fish, (both con- and heterospecific) from this area, 4) focusing spawns into a 1–2 m² area that he modifies by adding algae, and 5) remaining with the site day and night until the eggs hatch and the young disperse. This sequence of stages is similar to the evolutionary sequence suggested by previous theory, but differs in that site limitation is not necessary in order to lead to site attachment.     

基于交叉抚育的雄性根田鼠对异性同胞尿气味的识别

通过交叉抚育建立室内繁殖种群,在断奶后（80日龄）分别取这些供体的新鲜尿气味作刺激物,在行为观察箱中观察和记录雄性根田鼠对雌鼠气味的行为反应,以研究根田鼠同胞识别的化学通讯机制。结果表明：①在不同的发育时期（2～70日龄）,雄性同巢同胞与异巢同胞的体重没有显著差异。②雄性根田鼠对雌性同巢非同胞气味的接近潜伏期显著长于对异巢非同胞的接近潜伏期（P〈0．05）,其对异巢非同胞气味的访问时间和嗅舔时间都显著高于同巢非同胞气味（P〈0．05）。③雄性根田鼠对雌性异巢同胞和异巢非同胞气味的不存在明显偏好。其对两者的接近潜伏期、访问频次、访问时间、嗅舔频次和嗅舔时间等行为响应均无显著差异（P〈0．05）。这些结果表明,80日龄时,雄性根田鼠能够识别熟悉和陌生的无亲属关系雌性尿气味,但不能区分陌生的亲属和非亲属,因此,其异性同胞识别的机制为共生熟悉模式。     

Differences in Endogenous Levels of Gibberellin Activity in Male and Female Partners of Two Dioecious Tree Species

It was found that in two dioecious species, the carob (Ceratoniasiliqua) and the date palm (Phoenix dactylifera) growing intheir natural Mediterrancan habitat, the female partner invariablymanifested higher endogenous GN-like activity. While this trendwas consistent, marked seasonal fluctuations in both free andglycosidic bound-GN were observedhigher levels being associatedwith essentially vegetative spring growth and the converse associatedwith anthesis. It is postulated that while a clear correlationexists between female growth and high GN activity in these species,the switch from vegetative to generative growth in both themale and female may be associated with a lower relative proportionof endogenous GN in a specific multi-hormonal complex presumablyrequired for flower induction.     

Predation Risks and Anti-Predation Parental Care Behavior: An Experimental Study in a Tropical Skink

The process of parental care can be complex, and it is rarely exhibited by reptiles. How predators influence the timing of parental care is still ambiguous in terrestrial vertebrates. In this study, we demonstrate that female skinks of Mabuya longicaudata adjusted to an experimental manipulation of interspecific intruders which were placed into skink nests. When the intrusion frequency of the reptile-egg eating snake, Oligodon formosanus , increased, the time spent on maternal care by M. longicaudata was significantly extended. In contrast, female M. longicaudata recognized two sympatric lizards ( Sphenomorphus incognitus and Japalura swinhonis ) which do not prey upon eggs or adults of M. longicaudata and did not attack those species; consequently, the time spent on egg-guarding did not significantly differ from the control treatment with intrusion by S. incognitus or J. swinhonis . Mabuya longicaudata also recognized the predatory snake, Elaphe carinata , and when that species entered a skink nest, the skink escaped and never returned. These results emphasize that the time spent on parental care is probably influenced by predators, and the duration of this behavior is dependent on the maternal defensive capability. As egg guarding is the most basic and primitive form of parental care, the current study provides evidence possibly leading to insights into the origin of parental care from reptiles to birds and mammals.     

Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone,Dihydrotestosterone, and Glucocorticoids

Reproductive success is linked to dominance in male primates, reflecting the benefits of male competition. However, not all males compete successfully, suggesting that the costs of obtaining and maintaining high dominance status are significant. Here we examine the fecal metabolites of testosterone (fT) and dihydrotestosterone (fDHT) as bioactive androgens reflecting male reproductive effort, as well as fecal glucocorticoid (fGC) excretion as an index of stress in male white-faced capuchins (Cebus capucinus). We investigated the influence of female fertility (periovulatory vs. nonovulatory) on the hormonal responses of alpha and subordinate males. Over a 17-mo field season, we collected and analyzed weekly fecal samples (N = 992) from all 14 adult (> 10 yr) and subadult (≥ 6–10 yr) males residing in three study groups in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. Fecal samples (N > 2250) were also collected from group females (N = 28) to identify the fertile period using progesterone and estradiol assays. Alpha males had significantly higher fT, fDHT, and fGC levels than subordinate males independent of female reproductive state; further, adult subordinates had significantly higher fT, but not fDHT or fGC, than subadult subordinates. Male fT, fDHT, and fGC levels were significantly higher in the presence of fertile females, regardless of male dominance status and age. These findings indicate that the higher reproductive effort of alpha males comes with some costs (increased fGCs), and the presence of periovulatory females is associated with specific endocrine responses reflecting male reproductive effort and stress in white-faced capuchins.     

Allocation of Male Parental Care in Relation to Paternity Within and Among Broods of the Common Yellowthroat (Geothlypis trichas)

The relationship between male parental care and paternity has been investigated in a number of avian species, but in many cases the influences of confounding factors, such as variation in male and territory quality, were not addressed. These sources of variation can be controlled for by making within-male comparisons between successive broods or within-brood comparisons between groups of fledglings in a divided brood. We studied the relationship between male parental care and paternity in the common yellowthroat ( Geothlypis trichas ) at three levels: between groups of fledglings in divided broods, between first and second broods of the same pair, and among all broods in the population. In this study we proposed three hypotheses: first, males in double-brooded pairs should provide relatively more parental care to broods in which they have higher paternity; secondly, after fledging and brood division, males should provide more care to related offspring; and finally, among all broods in the population, paternity should be related positively to male parental care. Brood division occurred in many of the broods studied; however, broods were not divided according to fledgling size or paternity. Furthermore, within divided broods, males fed within-pair and extra-pair fledglings at similar rates. For sequential broods of the same pair, male feeding rates were not associated with differences in paternity between broods. Among all broods in the population, males did not provide relatively less care to broods containing unrelated young. The lack of a relationship between male parental care and paternity suggests that either males cannot assess their paternity or the costs of reducing male parental care outweigh the benefits.