Variation In Maternal Investment Research Articles

Geographic variation in maternal investment and trade-offs between egg size and clutch size in an endemic toad of the Qinghai-Tibet Plateau

Life history theory predicts that animals often produce fewer offspring of larger size and indicate a stronger trade-off between the number and size of offspring to cope with increasing environmental stress. In order to evaluate this prediction, we tested the life history characteristics of Bufo minshanicus at eight different altitudes on the eastern Tibetan Plateau, China. Our results revealed a positive correlation between female SVL and clutch size or egg size, revealing that larger females produce more and larger eggs. However, high-altitude toads seem to favor more offspring and smaller egg sizes when removing the effect of female SVL, which is counter to theoretical predictions. In addition, there was an overall significantly negative relationship between egg size and clutch size, indicative of a trade-off between egg size and fecundity. Therefore, we suggest that higher fecundity, rather than larger egg size, is a more effective reproductive strategy for this species of anuran living at high-altitude environments.

Effects of Maternal Reproductive Investment on Sex-Specific Pollutant Accumulation in Seabirds: A Meta-Analysis.

Avian egg production demands resources such as lipids and proteins. Relative egg size and mass varies across species, reflecting differences in maternal investment. This variability may affect the maternal transfer of anthropogenic pollutants including lipophilic polychlorinated biphenyls (PCBs) and protein-associated per- and polyfluoroalkyl substances (PFASs) and mercury (Hg). We conducted a meta-analysis on seabirds and investigated whether interspecies variation in maternal investment contributes toward skewed pollutant concentration ratios between males and females, as Cmale/Cfemale (80 studies). Overall concentrations of PCBs and perfluorooctanesulfonic acid (PFOS) were 1.6 and 1.3 times higher, respectively, in males than females, whereas mercury was similar between sexes. Few studies compared females and eggs ( n = 6), highlighting a knowledge gap. We found that an increasing maternal investment as a clutch-to-female mass ratio resulted in lower PCB concentrations in females than in males during the incubation period, but no sex-specific differences were observed for mercury and PFOS. Egg production is both a lipid dominated and protein-limited process. Females transfer lipophilic pollutants more easily to eggs, and to a higher degree with increasing maternal investment, but feeding ecology may be more important. Interspecies variation in maternal pollutant transfer may lead to negative effects scaling from an offspring to population level.

On the importance of having a good mother: maternal investment affects duckling mortality risk in wood ducks

Most avian populations experience more variation in recruitment than adult survival, and this drives much of the change in population growth rates from year to year. In duck species, the probability of duckling survival is an important component of recruitment into the breeding population. We investigated how variation in maternal investment in offspring by nesting female wood duck Aix sponsa affected duckling mortality (1‐survival) to 60 days of age using capture‐mark‐recapture techniques. Our primary sample consisted of 3035 ducklings, from 545 nests, that were marked with uniquely coded webtags on the day of hatch over nine nesting seasons (2008–2016). We also included 4437 hatch‐year and after‐hatch‐year individuals to increase precision on parameter estimates because some ducklings were not recaptured until after fledging. Duckling mortality was greatest during the first week of life and approached zero by the second week after hatching. We observed a quadratic effect of hatch date on duckling mortality suggesting that successful females improve fitness by nesting early in the year, but not too early (15 days before mean hatch). Increased egg volume and duckling mass reduced the probability of ducking mortality. Our results suggest that risk of mortality for ducklings is influenced, at least in part, by maternal effects, which are manifested through energy allocation and behavior during the breeding season. As such, individual heterogeneity among breeding females affects duckling mortality risk and likely the recruitment process for wood ducks.

Artificial selection reveals the energetic expense of producing larger eggs.

BackgroundThe amount of resources provided by the mother before birth has important and long-lasting effects on offspring fitness. Despite this, there is a large amount of variation in maternal investment seen in natural populations. Life-history theory predicts that this variation is maintained through a trade-off between the benefits of high maternal investment for the offspring and the costs of high investment for the mother. However, the proximate mechanisms underlying these costs of reproduction are not well understood. Here we used artificial selection for high and low maternal egg investment in a precocial bird, the Japanese quail (Coturnix japonica) to quantify costs of maternal reproductive investment.ResultsWe show that females from the high maternal investment lines had significantly larger reproductive organs, which explained their overall larger body mass, and resulted in a higher resting metabolic rate (RMR). Contrary to our expectations, this increase in metabolic activity did not lead to a higher level of oxidative damage.ConclusionsThis study is the first to provide experimental evidence for metabolic costs of increased per offspring investment.

Access to multiple mates increases fecundity but does not affect per-offspring maternal investment in a marine gastropod

Females of many organisms mate more than once and with more than one male, suggesting that polyandry confers some advantage to the female or her offspring. However, variation in maternal investment in response to mate choice and mate number can confound efforts to determine if there are benefits of polyandry. Access to multiple mates could increase maternal investment in offspring via a number of different mechanisms. Few studies have determined if investment is influenced by mate choice and number, and data are particularly lacking for marine invertebrates. This study was designed to determine if maternal investment and offspring size increase with access to increasing numbers of mates in the protandrous intertidal slipper snail Crepidula cf. marginalis. Virgin female slipper limpets were exposed to one, three, or five potential mates and their fecundity, egg size, and hatchling size were measured for multiple clutches. Treatment had a significant effect on fecundity, with fecundity increasing with the number of potential mates. Treatment did not have an effect on the size of eggs or hatchlings, on the variation in egg size or hatchling size within broods, or on the frequency of oviposition. Treatment did alter the variation in average offspring size among females, but not in the way predicted by theory. The main result, that access to multiple mates does not have an effect on per offspring maternal investment, makes C. cf. marginalis an ideal candidate to study the effects of polyandry on offspring fitness without having to take into account confounding effects of variation in maternal investment.

Natural selection acts in opposite ways on correlated hormonal mediators of prenatal maternal effects in a wild bird population.

Maternal hormones are important mediators of prenatal maternal effects. Although many experimental studies have demonstrated their potency in shaping offspring phenotypes, we know remarkably little about their adaptive value. Using long-term data on a wild collared flycatcher (Ficedula albicollis) population, we show that natural selection acts in opposite ways on two maternally derived androgens, yolk androstenedione (A4) and yolk testosterone (T). High yolk A4 concentrations are associated with higher fitness, whereas high yolk T concentrations are associated with lower fitness. Natural selection thus favours females that produce eggs with high A4 and low T concentrations. Importantly, however, there exists a positive (non-genetic) correlation between A4 and T, which suggests that females are limited in their ability to reach this adaptive optimum. Thereby, these results provide strong evidence for an adaptive value of differential maternal androgen deposition, and a mechanistic explanation for the maintenance of variation in maternal investment in the wild.

Maternal effects are long-lasting and influence female offspring's reproductive strategy in the swordtail fish Xiphophorus multilineatus.

The adaptive benefits of maternal investment into individual offspring (inherited environmental effects) will be shaped by selection on mothers as well as their offspring, often across variable environments. We examined how a mother's nutritional environment interacted with her offspring's nutritional and social environment in Xiphophorus multilineatus, a live-bearing fish. Fry from mothers reared on two different nutritional diets (HQ=high quality and LQ=low quality) were all reared on a LQ diet in addition to being split between two social treatments: exposed to a large adult male during development and not exposed. Mothers raised on a HQ diet produce offspring that were not only initially larger (at 14 days of age), but grew faster, and were larger at sexual maturity. Male offspring from mothers raised on both diets responded to the exposure to courter males by growing faster; however, the response of their sisters varied with mother's diet; females from HQ diet mothers reduced growth if exposed to a courter male, whereas females from LQ diet mothers increased growth. Therefore, we detected variation in maternal investment depending on female size and diet, and the effects of this variation on offspring were long-lasting and sex specific. Our results support the maternal stress hypothesis, with selection on mothers to reduce investment in low-quality environments. In addition, the interaction we detected between the mother's nutritional environment and the female offspring's social environment suggests that female offspring adopted different reproductive strategies depending on maternal investment.

Altitudinal variation in maternal investment and trade‐offs between egg size and clutch size in the Andrew's toad

AbstractEnvironmental variation along altitudinal gradients can promote life‐history trait differentiation in ectothermic animals. Life‐history theory predicts that increased environmental stress results in a shift in reproductive allocation from offspring quantity to quality and a stronger trade‐off between egg size and clutch size. To test this prediction, we investigated patterns of variation in life‐history traits (i.e. age, body size, clutch size and egg size) among four populations of Bufo andrewsi from Baoxing County, western China, at different altitudes. We found that body size, age, egg size and total reproductive output, but not clutch size, differed between populations. Clutch size and total reproductive output increased with female size and age. However, egg size decreased with female size and did not change with female age. The egg size and clutch size trade‐off was evident for all populations except at lowest altitude, and the strength of trade‐off between egg size and clutch size increased with altitude. Our findings suggest that environmental constraints at high altitude select for investment in larger eggs at a cost of offspring number.

Survival costs of reproduction predict age-dependent variation in maternal investment

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.

Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae).

Developmental maternal effects are a potentially important source of phenotypic variation, but they can be difficult to distinguish from other environmental factors. This is an important distinction within the context of social evolution, because if variation in offspring helping behavior is due to maternal manipulation, social selection may act on maternal phenotypes, as well as those of offspring. Factors correlated with social castes have been linked to variation in developmental nutrition, which might provide opportunity for females to manipulate the social behavior of their offspring. Megalopta genalis is a mass-provisioning facultatively eusocial sweat bee for which production of males and females in social and solitary nests is concurrent and asynchronous. Female offspring may become either gynes (reproductive dispersers) or workers (non-reproductive helpers). We predicted that if maternal manipulation plays a role in M. genalis caste determination, investment in daughters should vary more than for sons. The mass and protein content of pollen stores provided to female offspring varied significantly more than those of males, but volume and sugar content did not. Sugar content varied more among female eggs in social nests than in solitary nests. Provisions were larger, with higher nutrient content, for female eggs and in social nests. Adult females and males show different patterns of allometry, and their investment ratio ranged from 1.23 to 1.69. Adult body weight varied more for females than males, possibly reflecting increased variation in maternal investment in female offspring. These differences are consistent with a role for maternal manipulation in the social plasticity observed in M. genalis.

Maternal investment and nutrient use affect phenotype of American alligator and domestic chicken hatchlings

Maternal investment by oviparous amniotes, in the form of yolk and albumen, and the mechanisms by which embryos use available energy and nutrients have a profound effect on embryo and, consequently, hatchling phenotype. Nutrient provisioning and uptake vary within and among oviparous taxa, avian and non-avian reptiles, due to differences and similarities in environment, behavior, and phylogeny. Eggs of crocodilians, the closest extant relatives to modern birds, are ideal models for examining modes of embryonic development, especially with regard to nutrient uptake, in non-avian reptiles and comparing them with those of birds. In this study, we investigated egg composition, embryo growth, and nutrient use in the domestic chicken ( Gallus gallus) and American alligator ( Alligator mississippiensis). We explored egg composition by separating and weighing components of fresh eggs. We measured embryo growth and nutrient usage by dissecting embryos and by obtaining samples of liquid from the amnion, digestive tract, and yolk sac throughout the last half of incubation. Variation in albumen mass contributed most to egg mass variation in chicken eggs, whereas alligator eggs were composed almost equally of yolk and albumen, although larger eggs contained proportionally more albumen and less yolk than smaller eggs. Both chicken and alligator albumen were mostly water (87% and 96%, respectively) although chicken albumen contained over three times more solid mass per gram than alligator albumen. In both species, yolk contained a high proportion of solids. Larger eggs produced larger hatchlings in both chickens and alligators, but albumen solids contributed to embryo mass only in chicken embryos. However, intact albumen proteins appeared in the stomach in embryos of both species. While the final disposition of albumen in alligators is unclear, variation in maternal investment of yolk at oviposition was responsible for nearly all of the variation in alligator hatchling phenotype, while both yolk and albumen contributed to chicken hatchling mass.

Early ontogenetic effects on song quality in the Bengalese finch (Lonchura striata var. domestica): laying order, sibling competition, and song syntax

Birdsong differs from other sexual traits in that the acquisition process involves learning. Especially in close-ended learning species like the Bengalese finch, conditions experienced during the critical song-learning period can have a profound influence on song quality. Therefore, to understand song evolution from a life-history perspective, we investigated early ontogenetic effects on song quality. In particular, we focused on maternal effects and sibling competition. In asynchronously hatching bird species, the age hierarchy among nestlings affects physical development due to competition for food; mothers may influence this competition by adjusting their investment in each egg according to its sequence in the laying order. To independently assess these effects, chicks of the Bengalese finch were cross-fostered so that the age hierarchies formed in fostered broods were independent of the laying order. Our results indicate that song quality partially reflects early ontogenetic conditions, whereas song duration and note-type repertoire were independent of either laying order or age hierarchy. The syntactical complexity of note order declined over the laying sequence. This finding suggests that the song learning ability is influenced by within-clutch variation in maternal investment toward eggs. Considering that song syntactical complexity is subject to female preference in the Bengalese finch, it is likely that maternal resource allocation strategies play a role in song evolution.

GEOGRAPHIC VARIATION IN MATERNAL INVESTMENT: ACIDITY AFFECTS EGG SIZE AND FECUNDITY IN RANA ARVALIS

Environmental-stress-mediated geographic variation in reproductive parameters has been little studied in natural vertebrate populations outside the context of climatic variation. Based on life-history theory, an increase in the degree of environmental stress experienced by a population should lead to (1) a shift in reproductive allocation from fecundity to offspring quality, (2) stronger trade-offs between reproductive parameters, and (3) changes in the relationship between female phenotype and maternal investment. To test these predictions, we investigated geographic variation in maternal investment of moor frogs (Rana arvalis) in relation to breeding site acidity (pH 4-8). We found that mean egg size increased and clutch size and total reproductive output (TRO) decreased with increasing acidity among 19 Swedish moor frog populations. Tests for variation and co-variation in maternal investment and female size and age in 233 females from a subset of four acid origin (AO) and four neutral origin (NO) populations revealed that clutch size and TRO increased with female size in both acid and neutral environments. However, in AO populations, egg size also increased with female size, and clutch size and TRO with female age, whereas in NO populations, egg size increased with female age. The strength of the egg-size-clutch-size tradeoff tended to be stronger in AO than in NO females as expected if the former experience stronger environmental constraints. All in all, these results suggest that environmental acidification selects for investment in larger eggs at a cost to fecundity, imposes negative effects on reproductive output, and alters the relationship between female phenotype and maternal investment.

Maternal investment results in better foal condition through increased play behaviour in horses

Play behaviour is widespread in mammals, but benefits to play have been difficult to demonstrate. Physical training is one of the many proposed hypotheses, suggesting that males and females should play differently, that increased maternal investment should lead to increases in play, and that increases in play should result in physical advantages. In a population of feral horses, Equus caballus, males and females did not differ in their play behaviour except that males initiated more of their play bouts than females. Maternal condition influenced play behaviour only in males, with sons of mothers in good condition playing more. However, when we controlled for maternal effects by comparing a son and a daughter of the same mother, daughters played more when their mother was in poor condition and sons played more when their mother was in good condition. Mothers of foals that played more lost more condition. Therefore, the difference in play behaviour could not be explained by offspring sex or maternal condition alone, but play behaviour mirrored variation in maternal investment. In addition, those individuals that played more survived better and had better body condition as yearlings despite weaning earlier. Since increased activity has been linked to enhanced musculoskeletal development in domestic horses, we suggest that play provides a link between increased maternal investment, increased body condition and future reproductive success in feral horses, and probably in other species.

Epigenetic Programming of Phenotypic Variations in Reproductive Strategies in the Rat Through Maternal Care

Studies across multiple organisms reveal considerable phenotypic variation in reproductive tactics. In some species, this variation is associated with maternal effects in which variation in maternal investment results in stable individual differences in reproductive function. Recent studies with the rat suggest that maternal effects can alter the function of neuroendocrine systems associated with female sexual behaviour as well as maternal behaviour. These maternal effects appear to be mediated by epigenetic modifications at the promoter for oestrogen receptor alpha (ERalpha) and subsequent effects on gene expression. The tissue-specific nature of such effects may underlie the co-ordinated variation in multiple forms of reproductive function, resulting in distinct reproductive strategies.

High Variability in Egg Size and Energetic Content Among Intertidal Mussels

Maternal investment is a fundamentally important parameter in life-history theory and models, yet the scales at which it varies (among individuals vs. among populations) is rarely reported. In this study, variability in attributes of eggs and early larvae of Mytilus californianus was examined from four sites spanning Point Conception, California, in June and September 2001. The effects of female, site, and month were examined for the following variables: egg volume (microl), egg energy content (microg carbon per egg), and initial larval size (microm). The only significant effect on both egg traits was that of female. Females differed by up to 57% in mean egg volume and 116% in mean egg energetic content. Although there were significant effects of rearing environment, female, site, and month on initial larval size, variability in larval length was small compared to the egg traits. Mean larval length was maximally 11% different among females. Neither female body weight nor length was correlated to mean offspring traits, and there were also no significant relationships between egg traits and initial larval size. The primary source of variation in maternal investment in this system appears to be among individual females rather than over space or time.

Consequences of natural variation in maternal investment and larval nutrition on larval growth of a marine polychaete

Growth rates and planktonic development periods of marine invertebrate larvae have important consequences for the ecology of marine invertebrates. The growth and development of the larvae of a common southern Australian polychaete was examined to determine whether it was limited by natural concentrations of planktonic food, and whether naturally occurring variation in maternal investment in offspring influenced larval growth and development. Larvae that were provided concentrated diets of natural planktonic food were larger than larvae that were provided with food at ambient concentrations, but both experimental groups of larvae reached developmental stages immediately preceding settlement at the same time. Thus, larval growth was limited at natural concentrations of planktonic food but larval development rates were unaffected. These trends were also apparent in larvae fed with different concentrations of laboratory cultured food. Maternal investment in offspring (eggs) was higher on average for larger females than for smaller females. Larvae developing from smaller eggs were also smaller before settlement than larvae developing from larger eggs. Both maternal investment in offspring and the extent to which larval growth is food limited may vary spatially and seasonally along the southern coastline of Australia owing to the yearly occurrence of nutrient-rich oceanographic upwellings.

Maternal investment in egg size: environment- and population-specific effects on offspring performance

Geographic variation in maternal investment in offspring size can be adaptive if differences in investment translate into improved offspring performance in the given environments. We compared two moor frog, Rana arvalis, populations in the laboratory to test the hypothesis that investment in large eggs in populations originating from stressful (acid) environments improves offspring performance when reared in stressful (acid) conditions. We found that large initial size (hatchling mass) had moderate to strong, environment-dependent positive effects on larval and metamorphic traits in the acidic origin population, but only weak effects in the neutral origin population. Our results suggest that interactions between environmental conditions and initial size can be important determinants of individual performance, and that investment in large eggs is adaptive in acid environments. These findings emphasize the role of maternal effects as adaptations to environmental stress.

Maternal effects of egg size on emuDromaius novaehollandiaeegg composition and hatchling phenotype

Parental investment in eggs and, consequently, in offspring can profoundly influence the phenotype, survival and ultimately evolutionary fitness of an organism. Avian eggs are excellent model systems to examine maternal allocation of energy translated through egg size variation. We used the natural range in emu Dromaius novaehollandiae egg size, from 400 g to >700 g, to examine the influence of maternal investment in eggs on the morphology and physiology of hatchlings. Female emus provisioned larger eggs with a greater absolute amount of energy, nutrients and water in the yolk and albumen. Variation in maternal investment was reflected in differences in hatchling size, which increased isometrically with egg size. Egg size also influenced the physiology of developing emu embryos, such that late-term embryonic metabolic rate was positively correlated with egg size and embryos developing in larger eggs consumed more yolk during development. Large eggs produced hatchlings that were both heavier (yolk-free wet and dry mass) and structurally larger (tibiotarsus and culmen lengths) than hatchlings emerging from smaller eggs. As with many other precocial birds, larger hatchlings also contained more water, which was reflected in a greater blood volume. However, blood osmolality, hemoglobin content and hematocrit did not vary with hatchling mass. Emu maternal investment in offspring, measured by egg size and composition, is significantly correlated with the morphology and physiology of hatchlings and, in turn, may influence the success of these organisms during the first days of the juvenile stage.

Trends in the maternal investment of harbour porpoises are uncoupled from the dynamics of their primary prey.

Harbour porpoises in the Bay of Fundy and Gulf of Maine feed primarily on Atlantic herring. Herring stocks have undergone dramatic fluctuations in abundance over the past three decades due to changes in fishing intensity. In order to understand the effects of these changes in prey abundance on the patterns of maternal investment, I examined interdecadal variation in the size of porpoise calves measured in August prior to weaning. Female harbour porpoises exhibited significant variation in maternal investment between 1970 and 1999. During the 1980s, females consumed more herring and produced larger calves. Surprisingly, however, this increased maternal investment occurred during the period of lowest prey abundance, perhaps because the herring stock assessment does not reflect the availability or quality of prey to female porpoises.