The evolution of parental care in stochastic environments

Parental care is of fundamental importance to understanding reproductive strategies and allocation decisions. Here, we explore how parental care strategies evolve in variable environments. Using a set of life-history trait trade-offs, we explore the relative costs and benefits of parental care in stochastic environments. Specifically, we consider the cases in which environmental variability results in varying adult death rates, egg death rates, reproductive rate and carrying capacity. Using a measure of fitness appropriate for stochastic environments, we find that parental care has the potential to evolve over a wide range of life-history characteristics when the environment is variable. A variable environment that affects adult or egg death rates can either increase or decrease the fitness of care relative to that in a constant environment, depending on the specific costs of care. Variability that affects carrying capacity or adult reproductive rate has negligible effects on the fitness associated with care. Increasing parental care across different life-history stages can increase fitness gains in variable environments. Costly investment in care is expected to affect the overall fitness benefits, the fitness optimum and rate of evolution of parental care. In general, we find that environmental variability, the life-history traits affected by such variability and the specific costs of care interact to determine whether care will be favoured in a variable environment and what levels of care will be selected.     

Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis

Anurans breed in a variety of aquatic habitats with contrasting levels of desiccation risk, which may result in selection for faster development during larval stages. Previous studies suggest that species in ephemeral ponds reduce their developmental times to minimize desiccation risks, although it is not clear how variation in desiccation risk affects developmental strategies in different species. Employing a comparative phylogenetic approach including data from published and unpublished studies encompassing 62 observations across 30 species, we tested if species breeding in ephemeral ponds (High risk) develop faster than those from permanent ponds (Low risk) and/or show increased developmental plasticity in response to drying conditions. Our analyses support shorter developmental times in High risk, primarily by decreasing body mass at metamorphosis. Plasticity in developmental times was small and did not differ between groups. However, accelerated development in High risk species generally resulted in reduced sizes at metamorphosis, while some Low risk species were able compensate this effect by increasing mean growth rates. Taken together, our results suggest that plastic responses in species breeding in ephemeral ponds are constrained by a general trade-off between development and growth rates.     

Effects of among-offspring relatedness on the origins and evolution of parental care and filial cannibalism

Parental care is expected to increase the likelihood of offspring survival at the cost of investment in future reproductive success. However, alternative parental behaviours, such as filial cannibalism, can decrease current reproductive success and consequently individual fitness. We evaluate the role of among-offspring relatedness on the evolution of parental care and filial cannibalism. Building on our previous work, we show how the evolution of care is influenced by the effect of among-offspring relatedness on both the strength of competition and filial cannibalism. When there is a positive relationship between among-offspring competition and relatedness, parental care will be favoured when among-offspring relatedness is relatively low, and the maintenance of both care and no-care strategies is expected. If the relationship between among-offspring competition and relatedness is negative, parental care is most strongly favoured when broods contain highly related offspring. Further, we highlight the range of conditions over which the level of this among-offspring relatedness can affect the co-occurrence of different care/no care and cannibalism/no cannibalism strategies. Coexistence of multiple strategies is independent of the effects of among-offspring relatedness on cannibalism but more likely when among-offspring relatedness and competition are positively associated.     

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.     

Development and the effects of extended parenting in the cold‐breeding burying beetle Nicrophorus sayi

1. Burying beetles (Nicrophorus spp.) provide an excellent model system to test predictions about the relationships between environment, life‐history and behaviour. All species in the genus display similar natural histories, breeding on vertebrate carcasses and providing parental care to developing offspring. However, variations in other aspects of species' ecologies provide a rich framework to examine the evolution of parental behaviours and other traits. 2. One little‐studied species, N. sayi, breeds in substantially colder temperatures than its congeners, creating a potentially harsh environment for offspring. Here, we examined the timing of reproductive and developmental events in this species, and also investigated the effects of removing parents on offspring performance. 3. We find that development is not only extremely slow in this species, but it is also delayed even in comparison to other burying beetles reared at similar temperatures. However, the presence of parents reduces the time that offspring take to leave the carcass. This decrease in development time does not appear to result in a trade‐off with mortality or body size. 4. From these results, we suggest that very slow development may be advantageous when living in a particularly cold environment. Additionally, one role of extended parental care may be to assist offspring in dealing with these harsh conditions, and to mitigate the potentially negative consequences of adopting such a slow life‐history strategy.     

The origin of parental care in relation to male and female life history

The evolution of maternal, paternal, and bi‐parental care has been the focus of a great deal of research. Males and females vary in basic life‐history characteristics (e.g., stage‐specific mortality, maturation) in ways that are unrelated to parental investment. Surprisingly, few studies have examined the effect of this variation in male and female life history on the evolution of care. Here, we use a theoretical approach to determine the sex‐specific life‐history characteristics that give rise to the origin of paternal, maternal, or bi‐parental care from an ancestral state of no care. Females initially invest more into each egg than males. Despite this inherent difference between the sexes, paternal, maternal, and bi‐parental care are equally likely when males and females are otherwise similar. Thus, sex differences in initial zygotic investment do not explain the origin of one pattern of care over another. However, sex differences in adult mortality, egg maturation rate, and juvenile survival affect the pattern of care that will be most likely to evolve. Maternal care is more likely if female adult mortality is high, whereas paternal care is more likely if male adult mortality is high. These findings suggest that basic life‐history differences between the sexes can alone explain the origin of maternal, paternal, and bi‐parental care. As a result, the influence of life‐history characteristics should be considered as a baseline scenario in studies examining the origin of care.     

Aspects of embryonic and postembryonic development of the Japanese freshwater crayfish Cambaroides japonicus (Crustacea, Decapoda) including a hypothesis on the evolution of maternal care in the Astacida

Little is known about the biology of the East Asian freshwater crayfish of the genus Cambaroides. Furthermore, the phylogenetic relationships of Cambaroides are controversial. To gain more information about East Asian crayfish and to shed some light on the phylogeny and evolution of freshwater crayfish, some aspects of the embryonic and postembryonic development of the Japanese freshwater crayfish species Cambaroides japonicus are described. The general appearance of the embryo and the growth zone consisting of about 40 ectoteloblasts correspond with the apomorphic pattern described for all other freshwater crayfish species. The occurrence of eight mesoteloblasts is a typical malacostracan character. In addition to the occurrence of freshwater crayfish apomorphies, such as a telson thread, the postembryonic development of C. japonicus follows the ground pattern of the Northern Hemisphere Astacoidea. In particular, some characteristics are in common with the postembryonic development of the Astacidae. These concern the shape of the telson of the juvenile stage 1 and the occurrence of plumose telson setae in juvenile stage 2. Furthermore, the recurved hooks of the hatchlings are lost in the juvenile stage 2, indicating an early independence of the juveniles from the mother. On the other hand, the early appearance of a spermatheca (annulus ventralis) is shared between C. japonicus and the other (American) Cambaridae. The hypothesis is developed that the evolutionary success of the different freshwater crayfish taxa might be related to the stepwise extension of maternal care as an adaptation to the freshwater environment.     

Irreversible transfer of brood care duties and insights into the burden of caregiving in incipient subterranean termite colonies

1. In incipient termite colonies, biparental brood care rapidly shifts towards alloparental brood care. This transition was suggested to recapitulate the evolutionary trajectory from subsocial wood roach ancestors to eusociality in termites. 2. Incipient colonies of the subterranean termite Coptotermes gestroi (Wasmann) were investigated to determine if this transition was irreversible and if the burden of brood care on the first alloparents could be measured. To do so, the initial size of the work force necessary for an incipient colony to survive once the brood care became alloparental was determined. 3. The results of the study show that within 5 months after foundation, brood care duties were fully transferred to workers and the primary reproductives became irreversibly dependent on these workers for survival, reproduction, and colony growth. 4. Once the brood care became strictly alloparental, the presence of a single worker was enough to maintain the survival of the king and queen, confirming that ‘reversed parental care’ was also achieved. However, major brood loss and suppressed egg‐laying activity from the queen was observed, suggesting that the burden of brood care was too high for a single worker to absorb. Therefore, once brood care has shifted to alloparents, a critical number of workers is necessary to prevent brood loss and initiate colony growth. 5. As the initial cost of brood care is rapidly absorbed with colony growth in termites, the performance in brood care of the first few alloparents in a subsocial wood roach ancestor may have contributed to the emergence of eusociality in this clade.     

The role of fecundity and reproductive effort in defining life‐history strategies of North American freshwater mussels

Selection is expected to optimize reproductive investment resulting in characteristic trade‐offs among traits such as brood size, offspring size, somatic maintenance, and lifespan; relative patterns of energy allocation to these functions are important in defining life‐history strategies. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems, but little is known about their life‐history strategies, particularly patterns of fecundity and reproductive effort. Because mussels have an unusual life cycle in which larvae (glochidia) are obligate parasites on fishes, differences in host relationships are expected to influence patterns of reproductive output among species. I investigated fecundity and reproductive effort (RE) and their relationships to other life‐history traits for a taxonomically broad cross section of North American mussel diversity. Annual fecundity of North American mussel species spans nearly four orders of magnitude, ranging from < 2000 to 10 million, but most species have considerably lower fecundity than previous generalizations, which portrayed the group as having uniformly high fecundity (e.g. > 200000). Estimates of RE also were highly variable, ranging among species from 0.06 to 25.4%. Median fecundity and RE differed among phylogenetic groups, but patterns for these two traits differed in several ways. For example, the tribe Anodontini had relatively low median fecundity but had the highest RE of any group. Within and among species, body size was a strong predictor of fecundity and explained a high percentage of variation in fecundity among species. Fecundity showed little relationship to other life‐history traits including glochidial size, lifespan, brooding strategies, or host strategies. The only apparent trade‐off evident among these traits was the extraordinarily high fecundity of Leptodea, Margaritifera, and Truncilla, which may come at a cost of greatly reduced glochidial size; there was no relationship between fecundity and glochidial size for the remaining 61 species in the dataset. In contrast to fecundity, RE showed evidence of a strong trade‐off with lifespan, which was negatively related to RE. The raw number of glochidia produced may be determined primarily by physical and energetic constraints rather than selection for optimal output based on differences in host strategies or other traits. By integrating traits such as body size, glochidial size, and fecundity, RE appears more useful in defining mussel life‐history strategies. Combined with trade‐offs between other traits such as growth, lifespan, and age at maturity, differences in RE among species depict a broad continuum of divergent strategies ranging from strongly r‐selected species (e.g. tribe Anodontini and some Lampsilini) to K‐selected species (e.g. tribes Pleurobemini and Quadrulini; family Margaritiferidae). Future studies of reproductive effort in an environmental and life‐history context will be useful for understanding the explosive radiation of this group of animals in North America and will aid in the development of effective conservation strategies.     

Migratory life history of European eel Anguilla anguilla from freshwater regions of the River Asi, southern Turkey and their high otolith Sr:Ca ratios

Otolith Sr:Ca ratios from 32 of 34 European eel Anguilla anguilla collected from three freshwater sites in the River Asi, southern Turkey, indicated that they were resident in fresh water without apparent exposure to salt water since the elver stage. The Sr:Ca ratio criterion indicative of residence in fresh water was more than twice that of values from other European countries. Otolith Sr:Ca ratios of A. anguilla from fresh waters can vary among regions, possibly reflecting regional-specific water chemistry. Hence, the use of Sr:Ca ratios determined in one region to interpret results from a different region might lead to misclassification of migratory life-history types.     

Testing the role of phenotypic plasticity for local adaptation: growth and development in time-constrained Rana temporaria populations

Phenotypic plasticity can be important for local adaptation, because it enables individuals to survive in a novel environment until genetic changes have been accumulated by genetic accommodation. By analysing the relationship between development rate and growth rate, it can be determined whether plasticity in life-history traits is caused by changed physiology or behaviour. We extended this to examine whether plasticity had been aiding local adaptation, by investigating whether the plastic response had been fixed in locally adapted populations. Tadpoles from island populations of Rana temporaria, locally adapted to different pool-drying regimes, were monitored in a common garden. Individual differences in development rate were caused by different foraging efficiency. However, developmental plasticity was physiologically mediated by trading off growth against development rate. Surprisingly, plasticity has not aided local adaptation to time-stressed environments, because local adaptation was not caused by genetic assimilation but on selection on the standing genetic variation in development time.     

Food availability as a major driver in the evolution of life‐history strategies of sibling species

Life‐history theory predicts trade‐offs between reproductive and survival traits such that different strategies or environmental constraints may yield comparable lifetime reproductive success among conspecifics. Food availability is one of the most important environmental factors shaping developmental processes. It notably affects key life‐history components such as reproduction and survival prospect. We investigated whether food resource availability could also operate as an ultimate driver of life‐history strategy variation between species. During 13 years, we marked and recaptured young and adult sibling mouse‐eared bats (Myotis myotis and Myotis blythii) at sympatric colonial sites. We tested whether distinct, species‐specific trophic niches and food availability patterns may drive interspecific differences in key life‐history components such as age at first reproduction and survival. We took advantage of a quasi‐experimental setting in which prey availability for the two species varies between years (pulse vs. nonpulse resource years), modeling mark‐recapture data for demographic comparisons. Prey availability dictated both adult survival and age at first reproduction. The bat species facing a more abundant and predictable food supply early in the season started its reproductive life earlier and showed a lower adult survival probability than the species subjected to more limited and less predictable food supply, while lifetime reproductive success was comparable in both species. The observed life‐history trade‐off indicates that temporal patterns in food availability can drive evolutionary divergence in life‐history strategies among sympatric sibling species.     

Context-dependent development of sexual ornamentation: implications for a trade-off between current and future breeding efforts

Allocation of resources into the development of sexual displays is determined by a trade-off between the competing demands of current reproduction and self-maintenance. When reproduction overlaps with acquisition of sexual ornamentation, such as in birds with a yearly post-breeding moult, such a trade-off can be expressed in elaboration of sexual traits used in subsequent matings. In turn, selection for elaboration of sexual ornaments should favour resolution of this trade-off through a modification of the ornaments' development, resulting in variable and life history-dependent development of sexual displays. Here we examined a novel hypothesis that the trade-off between current reproduction and development of sexual ornamentation in the house finch (Carpodacus mexicanus) can be mediated by the shared effects of prolactin - a pituitary hormone that regulates both parental care and moult in this species. We compared developmental variation in sexual ornamentation between breeding, nonbreeding, and juvenile males and examined the relative contribution of residual levels of prolactin and individual condition during moult to the acquisition of sexual ornamentation. Males that invested heavily in parental care entered post-breeding moult in lower condition and later in the season, but their higher plasma prolactin was associated with shorter and more intense moult ultimately resulting in equal or greater elaboration of sexual ornamentation compared with nonparental males. Elaboration of sexual ornamentation of nonparental males that entered moult in greater condition, but with lower prolactin, was produced by longer and earlier moult and by lesser overlap in moult between sexual ornaments. Ornamentation of juvenile males that acquire sexual ornamentation for the first time was closely associated with physiological condition during moult. We discuss the implications of such context-dependent ontogenies of sexual ornamentation and resulting differences in condition-dependence of sexual traits across life history stages on the evolution of female preference for elaborated sexual displays.     

Morphological convergence during pregnancy among predator and nonpredator populations of the livebearing fish Brachyrhaphis rhabdophora (Teleostei: Poeciliidae)

Predation can drive morphological divergence in prey populations, although examples of divergent selection are typically limited to nonreproductive individuals. In livebearing females, shape often changes drastically during pregnancy, reducing speed and mobility and enhancing susceptibility to predation. In the present study, we document morphological divergence among populations of nonreproductive female livebearing fish (Brachyrhaphis rhabdophora) in predator and nonpredator environments. We then test the hypothesis that shape differences among nonreproductive females are maintained among reproductive females between predator and nonpredator environments. Nonreproductive females in predator environments had larger caudal regions and more fusiform bodies than females in nonpredator environments; traits that are associated with burst speed in fish. Shape differences were maintained in reproductive females, although the magnitude of this difference declined relative to nonreproductive females, suggesting morphological convergence during pregnancy. Phenotypic change vector analysis revealed that females in predator environments became more similar to females in nonpredator environments in the transition from nonreproductive to reproductive. Furthermore, the level of reproductive allocation affected shape similarly between predator environments. These results suggest a life‐history constraint on morphology, in which predator‐driven morphological divergence among nonreproductive B. rhabdophora is not maintained at the same level during pregnancy. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 386–392.     

Complex offspring size effects: variations across life stages and between species

Classical optimality models of offspring size and number assume a monotonically increasing relationship between offspring size and performance. In aquatic organisms with complex life cycles, the size–performance function is particularly hard to grasp because measures of performance are varied and their relationships with size may not be consistent throughout early ontogeny. Here, we examine size effects in premetamorphic (larval) and postmetamorphic (juvenile) stages of brooding marine animals and show that they vary contextually in strength and direction during ontogeny and among species. Larger offspring of the sea anemone Urticina felina generally outperformed small siblings at the larval stage (i.e., greater settlement and survival rates under suboptimal conditions). However, results differed when analyses were conducted at the intrabrood versus across‐brood levels, suggesting that the relationship between larval size and performance is mediated by parentage. At the juvenile stage (15 months), small offspring were less susceptible than large ones to predation by subadult nudibranchs and both sizes performed similarly when facing adult nudibranchs. In a sympatric species with a different life history (Aulactinia stella), all juveniles suffered similar predation rates by subadult nudibranchs, but smaller juveniles performed better (lower mortalities) when facing adult nudibranchs. Size differences in premetamorphic performance of U. felina were linked to total lipid contents of larvae, whereas size‐specific predation of juvenile stages followed the general predictions of the optimal foraging strategy. These findings emphasize the challenge in gathering empirical support for a positive monotonic size–performance function in taxa that exhibit complex life cycles, which are dominant in the sea.     

The evolution of parental care in shorebirds: life histories, ecology, and sexual selection

Parental care is expected to evolve according to a trade-offbetween the benefits of increased survival of offspring andcosts of reduced survival and future reproduction of adults.Here we investigate the components of this life-history trade-offin shorebirds (Charadriides, excluding Laroidea), an avian infraorderdisplaying an unusual diversity in extent of care by each sex.We show that evolutionary increases in the duration of carein one sex are associated with decreased care by the other.We found no evidence that various hypothesised benefits of careprovide a general explanation for the duration of care by eitheror both sexes, although parental feeding of the young was tooconservative for comparisons. Sexual dimorphism in body sizehad a similar relationship to parental care in both sexes: reductionsin duration of care by either sex were matched by increasesin the size of that sex relative to the other. Whereas thispattern could be explained by sexual selection in males, itwas retained within socially monogamous females. Reduced carein males (but not in females) appears to have facilitated theevolution of greater migration distances. These results suggestthat parental care has had different causes and consequencesin each sex. Benefits of desertion due to sexual selection aremore clearly demonstrable for males, whereas correlates of careare less clear for females     

Longitudinal observations of care and development of infant titi monkeys (Callicebus moloch)

The purpose of this study was to describe patterns of infant care and development in family groups of the monogamous titi (Callicebus moloch). Three infant titis were observed with their natal family groups over the first six months of life. Field observations of extensive male involvement with infants were confirmed. Adult males were clearly the infants' primary social companions, and infants spent more time in contact with adult males at all ages than with mothers or older siblings. However, mothers and siblings also carried infants at times and interacted with them in affiliative ways (e.g., grooming, nuzzling, play). Mothers often invited nursing, but otherwise it was infants who primarily initiated transfers between carriers and approaches to parents, reminding us that the infants' own activities and their effects on caregivers should not be overlooked in considerations of the patterns of infant care. This is particularly important for those species exhibiting extensive parental involvement by males. It is suggested that substantial male care of young titi infants leads to several important consequences for the infant's social development, including the development of a stronger attachment to the father than the mother.