The pay‐offs of maternal care increase as offspring develop,favouring extended provisioning in an egg‐feeding frog

Offspring quantity and quality are components of parental fitness that cannot be maximized simultaneously. When the benefits of investing in offspring quality decline, parents are expected to shift investment towards offspring quantity (other reproductive opportunities). Even when mothers retain complete control of resource allocation, offspring control whether to allocate investment to growth or development towards independence, and this shared control may generate parent–offspring conflict over the duration of care. We examined these predictions by, in a captive colony, experimentally removing tadpoles of the strawberry poison frog (Oophaga pumilio) from the mothers that provision them with trophic eggs throughout development. Tadpoles removed from their mothers were no less likely to survive to nutritional independence (i.e. through metamorphosis) than were those that remained with their mothers, but these offspring were smaller at metamorphosis and were less likely to survive to reach adult size, even though they were fed ad libitum. Tadpoles that remained with their mothers developed more slowly than those not receiving care, a pattern that might suggest that offspring extracted more care than was in mothers’ best interests. However, the fitness returns of providing care increased with offspring development, suggesting that mothers would be best off continuing care until tadpoles initiated metamorphosis. Although the benefits of parental investment in offspring quality are often thought to asymptote at high levels, driving parent–offspring conflict over weaning, this assumption may not hold over natural ranges of investment, with selection on both parents and offspring favouring extended durations of parental care.     

Cannibalism as a selective force on offspring size in fish

Cannibalism may cause considerable mortality on juvenile fish and it has been hypothesised that it may exercise selection on offspring size in that larger offspring may enjoy a size refuge. For this to be evolutionarily advantageous the survival of individual offspring must compensate for the reduced fecundity implied by larger offspring size. We develop a model which combines standard assumptions of size‐dependent mortality with adult cannibalism to investigate the potential for cannibalism to act as selective force on offspring size. We find that for this potential to be realised, the mortality due to cannibalism must exceed a threshold value that is a decreasing function of non‐cannibalistic predation intensity, cannibalized size range width and the average cannibalized size. If cannibalism exceeds this threshold, the model predicts evolution of offspring size towards refuges above or below cannibalized size range depending on initial offspring size. Cannibalistic mortality cannot be so great that the population is non‐viable, however, the range of parameter values describing cannibalistic intensity allowed within these boundaries is wide. On this basis, we suggest that cannibalism is a potential mechanism for offspring size selection.     

INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

Sexual and lifetime selection on body size in a marine fish: the importance of life-history trade-offs

Many field measurements of viability and sexual selection on body size indicate that large size is favoured. However, life-history theory predicts that body size may be optimized and that patterns of selection may often be stabilizing rather than directional. One reason for this discrepancy may be that field estimates of selection tend to focus on limited components of fitness and may not fully measure life-history trade-offs. We use an 8-year, demographic field study to examine both sexual selection and lifetime selection on body size of a coral reef fish (the bicolour damselfish, Stegastes partitus). Selection via reproductive success of adults was very strong (standardized selection differential=1.04). However, this effect was balanced by trade-offs between large adult size and reduced cumulative survival during the juvenile phase. When we measured lifetime fitness (net reproductive rate), selection was strongly stabilizing and only weakly directional, consistent with predictions from life-history theory.     

An integrated approach to life-cycle evolution using selective landscapes

A model which defines fitness in terms of the intrinsic rate of increase of phenotypes is used to analyse which life cycles are appropriate to which ecological circumstances. The following predictions are made for asexual animals and those sexual animals producing on average more than one daughter per brood. If there are no behavioural or physiological interactions between variables, then number of offspring per breeding should be maximized, survival until first/next breeding should be maximized, and time to first/next breeding should be minimized. If interactions occur such that altering one life-cycle variable affects another, then there are trade-offs between variables and the optimum trade-off will maximize fitness.Number of offspring per breeding will generally affect adult survivorship until next breeding. Given certain reasonable assumptions about this trade-off, high juvenile survivorship selects towards semelparity (many offspring per brood), low juvenile survivorship selects towards iteroparity (few offspring per brood). If juvenile survival depends on adult feeding, as in altricial birds, then juvenile survivorship declines as clutch size is increased. Optimal clutch size maximizes the number of surviving offspring per brood.Two trade-offs involve parental care. If parents guard their offspring they should take more risks if brood size is larger. The amount that parents feed their offspring should depend on how effective feeding is in enhancing growth. Growth may also be enhanced by taking risks, in juveniles or adults. The extent of risk-taking should depend on how effective risk-taking is in enhancing growth.If the number of offspring per brood is related to growing conditions for offspring, the prediction is that more offspring per brood should be produced if growing conditions for offspring are better. If the adult can protect the offspring, for example by encapsulating them, the amount of protection provided should depend on how effective the protection is in increasing offspring survivorship.     

Mothers determine offspring size in response to own juvenile growth conditions

Through non-genetic maternal effects, mothers can tailor offspring phenotype to the environment in which young will grow up. If juvenile and adult ecologies differ, the conditions mothers experienced as juveniles may better predict their offspring's environment than the adult environment of mothers. In this case maternal decisions about investment in offspring quality should already be determined during the juvenile phase of mothers. I tested this hypothesis by manipulating juvenile and adult maternal environments independently in a cichlid fish. Females raised in a poor environment produced larger young than females raised without food limitations, irrespective of the feeding conditions experienced during adulthood. This maternal boost was due to a higher investment in eggs and to faster larval growth. Apparently, mothers prepare their offspring for similar environmental conditions to those they encountered as juveniles. This explanation is supported by the distribution of these fishes under natural conditions. Juveniles live in a different and much narrower range of habitats than adults. Therefore, the habitat mothers experienced as juveniles will allow them to predict their offspring's environment better than the conditions in the adult home range.     

Benefits of parental care: Do juvenile lizards obtain better‐quality habitat by remaining with their parents?

Abstract Evolutionary theory suggests that parental care is favoured by natural selection when the benefits to offspring fitness outweigh the costs of parental expenditure. The nature of such benefits may differ among species, however, especially in species reflecting independent evolutionary origins of parental care. Black rock skinks (Egernia saxatilis, Scincidae) of south‐eastern Australia are viviparous rock‐dwelling lizards with prolonged parent–offspring association; adult pairs vigorously defend their home range – and, when present, their offspring – against conspecifics. We addressed the hypothesis that, by remaining within their parents' (vigorously defended) home range, juveniles thereby obtain access to better‐quality habitats. Measurements of biologically significant variables (crevice size, sun exposure, vegetation cover) revealed little difference between shelter‐rocks used by solitary (‘orphan’) juveniles and those within family groups containing adults. Indeed, the only consistent differences involved larger (and therefore, less predator‐proof) crevices for juveniles within family groups than for solitary conspecifics. Our data thus falsify the hypothesis that parental care evolves because of benefits associated with habitat quality; instead, it appears that parental protection of juveniles against infanticidal conspecifics may be the most plausible benefit to parent–offspring association in this system.     

Models of parent-offspring conflict. V. Effects of the behaviour of the two parents

In the absence of any parent-offspring conflict, the total parental investment per offspring should be less when two parents collaborate in caring for the offspring than when only one parent invests. This does not necessarily mean that offspring fare less well when both parents invest. The ‘ideal’ amount of parental investment for an offspring to take is always greater than is ‘ideal’ for the parent to allocate (Trivers 1974). The offspring's optimum is higher if the offspring's action affects the reproductive success of only one parent and lower if both parents are affected (e.g. two-parent investment, or lifelong monogamy). The difference between the parental optimum and the offspring optimum depends on the mating system and on the form of conflict (between successive broods, or within broods), and prescribes a ‘conflict range’. The extent of conflict cannot be deduced solely from a knowledge of the average relatedness between siblings. The conflict is likely to be resolved by an ESS in which intermediate (compromise) levels of investment are paid out to offspring, which nevertheless continue to make costly demands for yet more investment. The degree of conflict can be measured by the extent to which offspring subject their parents to aggressive demands for extra investment, and is likely to be greater when two parents collaborate equally over investment than when only one parent invests. When only one parent invests, conflict is higher if sibling-competition is between siblings in the same broods (intra-brood) than when it is between progeny in successive broods (inter-brood). However, the reverse will tend to be the case when both parents invest equally.     

Maternal and environmental influences on egg size and juvenile life‐history traits in Pacific salmon

Life‐history traits such as fecundity and offspring size are shaped by investment trade‐offs faced by mothers and mediated by environmental conditions. We use a 21‐year time series for three populations of wild sockeye salmon (Oncorhynchus nerka) to test predictions for such trade‐offs and responses to conditions faced by females during migration, and offspring during incubation. In years when their 1100 km upstream migration was challenged by high water discharges, females that reached spawning streams had invested less in gonads by producing smaller but not fewer eggs. These smaller eggs produced lighter juveniles, and this effect was further amplified in years when the incubation water was warm. This latter result suggests that there should be selection for larger eggs to compensate in populations that consistently experience warm incubation temperatures. A comparison among 16 populations, with matching migration and rearing environments but different incubation environments (i.e., separate spawning streams), confirmed this prediction; smaller females produced larger eggs for their size in warmer creeks. Taken together, these results reveal how maternal phenotype and environmental conditions can shape patterns of reproductive investment and consequently juvenile fitness‐related traits within and among populations.     

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.     

Asynchronous hatching in the burying beetle,Nicrophorus quadripunctatus,maxmizes parental fitness

Life history theory predicts that natural selection favours parents who balance investment across offspring to maximize fitness. Theoretical studies have shown that the optimal level of parental investment from the offspring's perspective exceeds that of its parents, and the disparity between the two generates evolutionary conflict for the allocation of parental investment. In various species, the offspring hatch asynchronously. The age hierarchy of the offspring usually establishes competitive asymmetries within the brood and determines the allocation of parental investment among offspring. However, it is not clear whether the allocation of parental investment determined by hatching pattern is optimal for parent or offspring. Here, we manipulated the hatching pattern of the burying beetle Nicrophorus quadripunctatus to demonstrate the influence of hatching pattern on the allocation of parental investment. We found that the total weight of a brood was largest in the group that mimicked the natural hatching pattern, with the offspring skewed towards early hatchers. This increases parental fitness. However, hatching patterns with more later hatchers had heavier individual offspring weights, which increases offspring fitness, but this hatching pattern is not observed in the wild. Thus, our study suggests that the natural hatching pattern optimizes parental fitness, rather than offspring fitness.     

Offspring size and timing of hatching determine survival and reproductive output in a lizard

Selection on offspring size and timing of birth or hatching could have important consequences for maternal investment strategies. Here we show consistent viability selection on hatchling body length across 2 consecutive years in a lizard that lays several clutches per season. There was no effect of hatching date on survival to maturity. However, both early hatching and large hatchling size increased adult size, which has a positive effect on total reproductive output. Earlier hatching also led to an earlier onset of reproduction. Overall, increased survival probability for large hatchlings and a positive effect of clutch size on recruitment suggest consistent directional selection on both egg size and clutch size within and across years. Because offspring size and timing of hatching are strongly affected by environmental and maternal effects, there should be potential for strong transgenerational effects on reproductive output in this species. We briefly discuss the implications of these results for the evolutionary ecology of maternal investment and population fluctuations in short-lived lizards.     

Signalling of information that is neither cryptic nor private

It is commonly assumed that in order for animal signals to be advantageous, the information being signalled could not have been obtained otherwise, and is therefore ‘cryptic’ or ‘private’. Here, we suggest a scenario in which individuals can gain an advantage by signalling ‘public’ information that is neither cryptic nor private. In that scenario, signalling increases the efficiency with which that ‘public’ information is transmitted. We formalize our idea with a game in which offspring can signal their condition to their parents. Specifically, we consider a resource‐strapped parent who can only invest in one of its two offspring, and we allow offspring the chance to influence parental investment through a signal. A parent in the game seeks to invest in the higher‐quality offspring, which it could identify either through a publicly available cue, such as body size, or by relying on a signal provided by the offspring. We find that if the signal can convey information about offspring quality more efficiently than cues, then signalling of condition between offspring and parents can be favoured by selection, even though parents could potentially have acquired the same information from the cue. Our results suggest that the biological function of signals may be broader than currently considered, and provide a scenario where low cost signalling can be favoured. More generally, efficiency benefits could explain signalling across a range of biological and economic scenarios.     

The influence of mating system on the intensity of parent-offspring conflict in primates

An evolutionary conflict of interest exists between parents and their offspring over the partitioning of parental investment (PI) among siblings. When the direct fitness benefits to offspring of increased PI, outweigh the inclusive fitness costs from lost future sibling fitness, selection should favour the evolution of offspring selfishness over altruism. In theory, this conflict is heightened when females are not strictly monogamous, as current offspring should be less altruistic towards future half-siblings than they would be towards full-siblings. Using data collected on foetal growth rate (representing prenatal PI) in primates, I test the prediction from theory that the resolution of the parent-offspring conflict will be closer to the offspring's evolutionary optima in polyandrous species than in more monandrous species. Using phylogenetic comparative analysis, and controlling for allometry, I show that offspring are able to obtain more PI when the probability of future full-siblings decreases, and that this is most pronounced in taxa where there is the opportunity for direct foetal access to the maternal bloodstream. These results support the hypothesis that the resolution of prenatal PI conflict is influenced by both a species' mating system and by its placental structure.     

The influence of a positive correlation between clutch size and offspring fitness on the optimal offspring size

Summary The effect is modeled of a positive relationship between clutch size and offspring fitness on the optimal investment in offspring. In species which meet the assumptions of the model, the model predicts a positive correlation between maternal resource level and offspring size. If larger mothers are able to allocate more resources to offspring, then the model would also predict a positive correlation between maternal size and offspring size when the assumptions of the model are met. Thus, this model may help explain both among and within individual variation in offspring size. When offspring are produced in groups and the number of offspring killed per clutch is limited by predator satiation, offspring in larger clutches may experience a higher probability of survival. Such a life style may be found in animals such as sea turtles. Offspring size is positively correlated with maternal size in some members of this group.     

DO EMBRYOS INFLUENCE MATERNAL INVESTMENT? EVALUATING MATERNAL‐FETAL COADAPTATION AND THE POTENTIAL FOR PARENT‐OFFSPRING CONFLICT IN A PLACENTAL FISH

The evolution of matrotrophy introduces the potential for genomic conflicts between mothers and embryos. These conflicts are hypothesized to accelerate the evolution of reproductive isolation and to influence the evolution of life-history traits, reproductive structures, and genomic imprinting. These hypotheses assume offspring can influence the amount of maternal investment they receive and that there is a trade-off between maternal investment into individual offspring and maternal survival or fecundity. We used field data and laboratory crosses to test whether these assumptions are met in the matrotrophic poeciliid fish Heterandria formosa . Comparisons of life histories between two natural populations demonstrated a trade-off between the level of maternal investment into individual embryos and maternal fecundity. Laboratory crosses between individuals from these populations revealed that offspring genotype exerts an influence on the level of maternal investment and affects maternal fecundity through higher rates of embryo abortion and lower numbers of full-term offspring. Our results show that the prerequisites for parent–offspring conflict to be a potent evolutionary force in poeciliid fish are present in H. formosa. However, determining whether this conflict has shaped maternal investment in nature will require disentangling any effects of conflict from those of several ecological factors that are themselves correlated with the expected intensity of conflict.     

Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata

Abstract The existence of adaptive phenotypic plasticity demands that we study the evolution of reaction norms, rather than just the evolution of fixed traits. This approach requires the examination of functional relationships among traits not only in a single environment but across environments and between traits and plasticity itself. In this study, I examined the interplay of plasticity and local adaptation of offspring size in the Trinidadian guppy, Poecilia reticulata. Guppies respond to food restriction by growing and reproducing less but also by producing larger offspring. This plastic difference in offspring size is of the same order of magnitude as evolved genetic differences among populations. Larger offspring sizes are thought to have evolved as an adaptation to the competitive environment faced by newborn guppies in some environments. If plastic responses to maternal food limitation can achieve the same fitness benefit, then why has guppy offspring size evolved at all? To explore this question, I examined the plastic response to food level of females from two natural populations that experience different selective environments. My goals were to examine whether the plastic responses to food level varied between populations, test the consequences of maternal manipulation of offspring size for offspring fitness, and assess whether costs of plasticity exist that could account for the evolution of mean offspring size across populations. In each population, full‐sib sisters were exposed to either a low‐ or high‐food treatment. Females from both populations produced larger, leaner offspring in response to food limitation. However, the population that was thought to have a history of selection for larger offspring was less plastic in its investment per offspring in response to maternal mass, maternal food level, and fecundity than the population under selection for small offspring size. To test the consequences of maternal manipulation of offspring size for offspring fitness, I raised the offspring of low‐ and high‐food mothers in either low‐ or high‐food environments. No maternal effects were detected at high food levels, supporting the prediction that mothers should increase fecundity rather than offspring size in noncompetitive environments. For offspring raised under low food levels, maternal effects on juvenile size and male size at maturity varied significantly between populations, reflecting their initial differences in maternal manipulation of offspring size; nevertheless, in both populations, increased investment per offspring increased offspring fitness. Several correlates of plasticity in investment per offspring that could affect the evolution of offspring size in guppies were identified. Under low‐food conditions, mothers from more plastic families invested more in future reproduction and less in their own soma. Similarly, offspring from more plastic families were smaller as juveniles and female offspring reproduced earlier. These correlations suggest that a fixed, high level of investment per offspring might be favored over a plastic response in a chronically low‐resource environment or in an environment that selects for lower reproductive effort     

Sexual dimorphism is associated with population fitness in the seed beetle Callosobruchus maculatus

The population consequences of sexual selection remain empirically unexplored. Comparative studies, involving extinction risk, have yielded different results as to the effect of sexual selection on population densities make contrasting predictions. Here, we investigate the relationship between sexual dimorphism (SD) and population productivity in the seed beetle Callosobruchus maculatus, using 13 populations that have evolved in isolation. Geometric morphometric methods and image analysis are employed to form integrative measures of sexual dimorphism, composed of variation in weight, size, body shape, and pigmentation. We found a positive relationship between SD and adult fitness (net adult offspring production) across our study populations, but failed to find any association between SD and juvenile fitness (egg-to-adult survival). Several mechanisms may have contributed to the pattern found, and variance in sexual selection regimes across populations, either in female choice for "good genes" or in the magnitude of direct benefits provided by their mates, would tend to produce the pattern seen. However, our results suggest that evolutionary constraints in the form of intralocus sexual conflict may have been the major generator of the relationship seen between SD and population fitness.     

Selection and constraints on offspring size‐number trade‐offs in sand lizards (Lacerta agilis)

The trade‐off between offspring size and number is a central component of life‐history theory, postulating that larger investment into offspring size inevitably decreases offspring number. This trade‐off is generally discussed in terms of genetic, physiological or morphological constraints; however, as among‐individual differences can mask individual trade‐offs, the underlying mechanisms may be difficult to reveal. In this study, we use multivariate analyses to investigate whether there is a trade‐off between offspring size and number in a population of sand lizards by separating among‐ and within‐individual patterns using a 15‐year data set collected in the wild. We also explore the ecological and evolutionary causes and consequences of this trade‐off by investigating how a female's resource (condition)‐ vs. age‐related size (snout‐vent length) influences her investment into offspring size vs. number (OSN), whether these traits are heritable and under selection and whether the OSN trade‐off has a genetic component. We found a negative correlation between offspring size and number within individual females and physical constraints (size of body cavity) appear to limit the number of eggs that a female can produce. This suggests that the OSN trade‐off occurs due to resource constraints as a female continues to grow throughout life and, thus, produces larger clutches. In contrast to the assumptions of classic OSN theory, we did not detect selection on offspring size; however, there was directional selection for larger clutch sizes. The repeatabilities of both offspring size and number were low and we did not detect any additive genetic variance in either trait. This could be due to strong selection (past or current) on these life‐history traits, or to insufficient statistical power to detect significant additive genetic effects. Overall, the findings of this study are an important illustration of how analyses of within‐individual patterns can reveal trade‐offs and their underlying causes, with potential evolutionary and ecological consequences that are otherwise hidden by among‐individual variation.     

Optimal offspring sizes in small litters

Summary Numerous evolutionary models explore the trade-off between offspring size and offspring number. However, such models often fail when the number of offspring is small because optimal litter size (or litter size at optimal offspring size) may fall between the necessarily integer values for real litters. This paper extends a classic model for optimal investment per offspring to the case of small litters and predicts that range in offspring size and the largest (smallest) offspring size should decline (increase) with increased litter size. Application of the model to egg size data from a poeciliid fish,Gambusia hubbsi, reveals a surprisingly close approximation to the largest offspring size and variation in offspring size at small litter sizes.