Maternal Investment In Offspring Research Articles

Semen promotes oocyte development in Sebastes schlegelii elucidating ovarian development dynamics in live-bearing fish

In some vertebrates and invertebrates, semen release factors affecting female physiology and behavior. Here, we report that semen delivered to females is potentially beneficial for promoting oocyte development in a viviparous teleost, Sebastes schlegelii. 88% of mated ovaries develop normally and give birth to larval fish, whereas 61% of non-mated ovaries are arrested in the previtellogenic stage. Semen's significant role (p<0.0001) in promoting oocyte development may involve remodeling follicular cells and regulating the expression of the extracellular matrix, which facilitates cell communication. Furthermore, the ovarian response to semen may influence the brain, affecting hormone release, follicular cell development and steroid production, and crucial for oocyte growth. This mechanism, which could potentially delay maternal investment in offspring until male genetic input occurs to avoid energy wastage, has not been previously described in teleosts. These findings enhance our understanding of ovarian development in viviparous fish, with broader implications for reproductive biology.

Lipid and protein utilization during lecithotrophic development in the asteroid Stegnaster inflatus, with a review of larval provisioning in lecithotrophic echinoderms

The eggs of echinoderms with lecithotrophic development provide structural and nutritional materials (lipids, proteins) to complete development without any external sources of nutrition. Previous studies have suggested that a relatively large proportion of the maternal lipid reserves remain after settlement to provision the early post-metamorphic juvenile. Here we examined lipid and protein utilization during lecithotrophic development of the asterinid starfish Stegnaster inflatus which has large (~400 µm diameter), negatively buoyant eggs. S. inflatus produces eggs with a large amount of lipid (mean ± SD: 2047 ± 315 ng egg-1), with 26% structural lipids and 74% energetic lipids dominated by diacylglycerol ether (DAGE; 66%). Similar amounts of protein were present in the egg (mean ± SD: 2143 ± 157 ng egg-1), with a lipid:protein ratio of 0.96. Approximately 80% of the egg protein is used prior to settlement. In contrast, 51.0% of the energetic lipids provided in the egg, and 40.3% of the DAGE remain for provisioning of the early juvenile. A review of lecithotrophic development in echinoderms reveals that asteroid, echinoid and ophiuroid species have an excess of 50% of the maternal lipids remaining in the settled post-larva. When considering maternal investment in offspring for lecithotrophic developers, we need to consider energetic use during the short dispersal period, as well as provisioning for post-metamorphic early juvenile life.

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.

Parental phenotype not predator cues influence egg warning coloration and defence levels

In species that advertise their toxicity to predators through visual signals, there is considerable variation among individuals in both signal appearance and levels of defence. Parental effects, a type of nongenetic inheritance, may play a key role in creating and maintaining this within-species diversity in aposematic signals; however, a comprehensive test of this notion is lacking. Using the ladybird Adalia bipunctata, we assessed how egg coloration and defence level (concentration of the toxic alkaloid (-)-adaline) is influenced both by simulated predation risk in the egg-laying environment and by parental phenotype (coloration and toxin level). We found that egg toxin level and colour were predicted by parental phenotype but were not altered in response to cues of egg predators. Egg luminance (lightness) was positively correlated with paternal elytral luminance, while maternal toxin level positively predicted egg toxin level. In response to egg predator cues, ladybird mothers altered the timing of laying and total egg number, but not egg toxin level or colour. It appears therefore that in A. bipunctata variation between individuals of the same morph in the colour and toxin level of the eggs they lay, that is, egg aposematic phenotype, is more strongly influenced by individual variation in parental aposematic traits than by environmental cues of egg predation risk. Furthermore, these results provide the first indication that, in a warningly coloured species, male coloration may play a dual role as predator deterrent and indicator of paternal quality, influencing maternal investment in offspring.

Establishment of Legal Paternity for Children of Unmarried American Women : Trade-Offs in Male Commitment to Paternal Investment.

The establishment of a legal father for children of unmarried parents reflects both high paternity confidence and male willingness to commit to paternal investment. Whether an unmarried man voluntarily acknowledges paternity after a child is born has important consequences for both the mother and child. This paper brings to bear a life history perspective on paternity establishment, noting that men face trade-offs between mating and parental effort and that women will adjust their investment in children based on expected male investment. I predict that paternity establishment will be more likely when the mother has high socioeconomic status, when maternal health is good, and when the child is male, low parity, or a singleton (versus multiple) birth. I further predict that establishment of paternity will be associated with increased maternal investment in offspring, resulting in healthier babies with higher birthweights who are more likely to be breastfed. These predictions are tested using data on 5.4 million births in the United States from 2009 through 2013. Overall the results are consistent with the hypothesis that the trade-offs men face between reproductive and parental investment influence whether men voluntarily acknowledge paternity when a child is born.

Maternal effects on offspring size in a natural population of the viviparous tsetse fly

1. Theory predicts that mothers should adaptively adjust reproductive investment depending on current reserves and future reproductive opportunities. Females in better intrinsic state, or with more resources, should invest more in current reproduction than those with fewer resources. Across the lifespan, investment may increase as future reproductive opportunities decline, yet may also decline with reductions in intrinsic state.2. Across many species, larger mothers produce larger offspring, but there is no theoretical consensus on why this is so. This pattern may be driven by variation in maternal state such as nutrition, yet few studies measure both size and nutritional state or attempt to tease apart confounding effects of size and age.3. Viviparous tsetse flies (Glossina species) offer an excellent system to explore patterns of reproductive investment: females produce large, single offspring sequentially over the course of their relatively long life. Thus, per‐brood reproductive effort can be quantified by offspring size.4. While most tsetse reproduction research has been conducted on laboratory colonies, maternal investment was investigated in this study using a unique field method where mothers were collected as they deposited larvae, allowing simultaneous mother‐offspring measurements under natural conditions.5. It was found that larger mothers and those with a higher fat content produced larger offspring, and there was a trend for older mothers to produce slightly larger offspring.6. The present results highlight the importance of measuring maternal nutritional state, rather than size alone, when considering maternal investment in offspring. Implications for understanding vector population dynamics are also discussed.

Growth trajectories in wild geladas (Theropithecus gelada).

Life history and socioecological factors have been linked to species-specific patterns of growth across female vertebrates. For example, greater maternal investment in offspring has been associated with more discrete periods of growth and reproduction. However, in primates it has been difficult to test such hypotheses because very few studies have obtained growth measurements from wild populations. Here we utilize a promising noninvasive photogrammetric method-parallel lasers-to examine shoulder-rump (SR) growth in a wild primate, the gelada (Theropithecus gelada, Simien Mountains National Park, Ethiopia). In this species, a graminivorous diet coupled with high extrinsic infant mortality risk suggests that maternal investment in neonates is low. Therefore, in contrast with other closely related papionins, we expected female geladas to exhibit less discrete periods of growth and reproduction. For both sexes, we compared size-for-age patterns (N = 154 females; N = 110 males) and changes in growth velocity relative to major life history milestones. Female geladas finished 88.5% of SR growth by first sexual swelling, and 97.2% by first reproduction, reaching adult body size by 7.72 years of age. Compared to closely related papionins, gelada females finished more growth by first reproduction, despite producing relatively small, and presumably "cheap," neonates. Male geladas finished 85.4% of growth at dispersal, and 96.0% at estimated first birth. Contrary to other polygynous primates, males are larger than females because they grow for a longer period of time (not because they grow faster), surpassing females around 6 years of age when female growth slows. Our results demonstrate that parallel lasers are an easy and promising new method that can be used to construct comprehensive life history perspectives that were once out of reach for wild populations. Am. J. Primatol. 78:707-719, 2016. © 2016 Wiley Periodicals, Inc.

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.

Symbiont-Supplemented Maternal Investment Underpinning Host’s Ecological Adaptation

Maternal investment for offspring's growth and survival is widespread among diverse organisms. Vertical symbiont transmission via maternal passage is also pivotal for offspring's growth and survival in many organisms. Hence, it is expected that vertical symbiont transmission may coevolve with various organismal traits concerning maternal investment in offspring. Here we report a novel phenotypic syndrome entailing morphological, histological, behavioral, and ecological specializations for maternal investment and vertical symbiont transmission in stinkbugs of the family Urostylididae. Adult females develop huge ovaries exaggerated for polysaccharide excretion, possess novel ovipositor-associated organs for vertical transmission of a bacterial symbiont ("Candidatus Tachikawaea gelatinosa"), and lay eggs covered with voluminous symbiont-supplemented jelly. Newborns hatch in midwinter, feed solely on the jelly, acquire the symbiont, and grow during winter. In spring, the insects start feeding on plant sap, wherein the symbiont localizes to a specialized midgut region and supplies essential amino acids deficient in the host's diet. The reduced symbiont genome and host-symbiont cospeciation indicate their obligate association over evolutionary time. Experimental deprivation of the jelly results in nymphal mortality, whereas restoration of the jelly leads to recovered nymphal growth, confirming that the jelly supports nymphal growth in winter. Chemical analyses demonstrate that the galactan-based jelly contains a sufficient quantity of amino acids to sustain nymphal growth to the third instar. The versatile biological roles of the symbiont-containing egg-covering jelly highlight intricate evolutionary interactions between maternal resource investment and vertical symbiont transmission, which are commonly important for offspring's growth, survival, and ecological adaptation.

Reproductive demography of two closely related Emydine Turtles in a spring fed system

Freshwater turtles are appropriate organisms for studying maternal investment in offspring because, unlike most long-lived vertebrates, turtles show high fecundities and most provide no parental care. We studied reproductive patterns of two emydine freshwater turtle species, the Texas river cooter (Pseudemys texana) and the red-eared slider (Trachemys scripta elegans) at Spring Lake, Hays County, Texas during the 2009 nesting season. Forty-six percent of all nesting Texas river cooters and 25% of all nesting red-eared sliders nested twice, with some Texas river cooters nesting more than twice. Mean egg mass, egg length, and egg width decreased in subsequent clutches in Texas river cooters. However, there was an insufficient sample size of subsequent clutches (n = 6) to draw conclusions for red-eared sliders. Red-eared sliders did not show a positive relationship between clutch size and body size. We found that in both species there was a positive relationship between egg width and egg mass in relation to maternal body size. However, only Texas river cooters showed a positive relationship between clutch size and maternal size, while only red-eared sliders showed a positive relationship between egg length and maternal size. By comparing reproductive parameters of these two coexisting populations, we concluded that the members of these two species allocate resources differently for reproduction.

The Offspring-Development-Time/Offspring-Number Trade-Off

The metabolic theory of ecology (MTE) states that metabolic rate, ruled mainly by individual mass and temperature, determines many other biological rates. This view of ecology as ruled by the laws of physics and thermodynamics contrasts with life-history-optimization (LHO) theories, where traits are shaped by evolutionary processes. Integrating the MTE and LHO can lead, however, to a synthetic theory of ecology. In this work, we link the two theories to show that offspring development time is the result of both maternal investment in offspring and the metabolic constraints on offspring growth. We formulate a model that captures how offspring development time is the consequence of both offspring growth rate, determined by temperature and allometric scaling in accordance with the MTE, and the size reached by offspring at the end of the developmental period, determined mainly by LHO and reproductive strategies. We first extend the trade-off between offspring size and offspring number to ectotherms, showing that increased body temperatures result in increased resources available for reproduction. We then combine this trade-off with the general ontogenetic growth model to show that there is a trade-off between the number of offspring produced and offspring development time. The model predicts a shorter developmental time in organisms producing larger numbers of offspring.

Behavioral and Ecological Consequences of Sex‐Based Differences in Gustatory Anatomy in Cebus apella

Fungiform papillae (FPs) are the only gustatory structures on the anterior tongue. Taste buds (TBs), which are located in FPs, house taste receptors. Each TB has a taste pore (TP) by which tastants are transmitted. In humans, FP and TB densities correlate with taste sensitivity and food preferences. Females have higher FP densities than males in Homo, Pan, and Cebus. Homo, Pan, and Cebus also have larger brains, slower ontogenetic development, and higher maternal investment in offspring compared to most primates. An increase in maternal investment places intense pressure on females to 1) obtain high-quality foods, and 2) detect potential toxins at low levels. This study examines sex differences in FPs and TPs (a TB surrogate) in 11 Cebus apella to test the hypothesis that higher FP density in females may be an adaptation specific to reproductive strategies of females. Tongues were imaged using an environmental scanning electron microscope; from these images FP surface area, FP density, TP count, and TP densities were calculated. We found that there were no significant differences between males and females in the number of TPs per FP. However, we did find that females do have larger FP surface areas and higher FP densities than males. The anatomical evidence indicates that females may have greater taste sensitivity than males because females have more FP than males. Future research on food preference and selection in Cebus is expected to show sex-specific behaviors similar to those observed in Homo and Pan.

Food availability at birth limited reproductive success in historical humans

Environmental conditions in early life can profoundly affect individual development and have consequences for reproductive success. Limited food availability may be one of the reasons for this, but direct evidence linking variation in early-life nutrition to reproductive performance in adulthood in natural populations is sparse. We combined historical agricultural data with detailed demographic church records to investigate the effect of food availability around the time of birth on the reproductive success of 927 men and women born in 18th-century Finland. Our study population exhibits natural mortality and fertility rates typical of many preindustrial societies, and individuals experienced differing access to resources due to social stratification. We found that among both men and women born into landless families (i.e., with low access to resources), marital prospects, probability of reproduction, and offspring viability were all positively related to local crop yield during the birth year. Such effects were generally absent among those born into landowning families. Among landless individuals born when yields of the two main crops, rye and barley, were both below median, only 50% of adult males and 55% of adult females gained any reproductive success in their lifetime, whereas 97% and 95% of those born when both yields were above the median did so. Our results suggest that maternal investment in offspring in prenatal or early postnatal life may have profound implications for the evolutionary fitness of human offspring, particularly among those for which resources are more limiting. Our study adds support to the idea that early nutrition can limit reproductive success in natural animal populations, and provides the most direct evidence to date that this process applies to humans.

The Influence of Maternal Quality on Brood Sex Allocation in the Small Carpenter Bee, Ceratina calcarata

AbstractIn the twig‐nesting carpenter bee, Ceratina calcarata, body size is an important component of maternal quality, smaller mothers producing significantly fewer and smaller offspring than larger mothers. As mothers precisely control the sex and size of each offspring, smaller mothers might compensate by preferentially allocating their investment towards sons. We investigated whether variation in maternal quality leads to variation in sex allocation patterns. At the population level, the numerical sex ratio was 57% male‐biased (1.31 M/F), but the investment between the sexes was balanced (1.02 M/F), because females are 38% larger than males (1.28 F/M). Maternal body size explained both sex allocation pattern and size variation among offspring: larger mothers invested more in individual progeny and produced more female offspring than smaller mothers. Maternal investment in offspring of both sexes decreased throughout the season, probably as a result of increasing maternal wear and age. The exception to this pattern was the curious production of dwarf females in the first two brood cell positions. We suggest that the sex ratio distribution reflects the maternal body size distribution and a constraint on small mothers to produce small broods. This leads to male‐biased allocation by small females, to which large mothers respond by biasing their allocation towards daughters.

A Comparison of Female Mating Strategies in Pan troglodytes and Pongo spp.

Orangutans and chimpanzees differ in many aspects of their mating and social systems. Nevertheless, because both great apes require enormous maternal investment in offspring and because female reproductive potential is limited, female orangutans and chimpanzees should be selective of their mates, yet expected to exhibit anti-infanticide strategies such as mating with multiple males. We review and compare mating patterns in orangutans and chimpanzees to understand how these critical pressures are filtered through the different demands of the socioecology of each species. We highlight the variation in female mating behavior as a function of the proximity of ovulation. We conclude that both genera pursue tactics for paternity confusion by mating with multiple males and by mating cooperatively or even proceptively with nonpreferred partners when conception is unlikely. Mating selectivity is suggested by variation in proceptive behavior toward particular partners and by increased resistance of nonpreferred partners during the periovulatory period. Thus, data for both species support a mixed mating strategy whereby females shift their mating behavior in accordance with ovulatory status to accommodate the competing demands of mate selectivity and paternity confusion.

Maternal effects on offspring Igs and egg size in relation to natural and experimentally improved food supply

1. Maternal effects have been suggested to function as a mechanism for transgenerational plasticity, in which the environment experienced by the mother is translated into the phenotype of the offspring. In birds and other oviparous vertebrates where early development is within the egg, mothers may be able to improve the viability prospects of their offspring at hatching by priming eggs with immunological and nutritional components. 2. We studied how resource availability affects maternal investment in offspring by feeding Ural owl (Strix uralensis, Pall.) females prior to egg-laying in 3 years of dramatically different natural food conditions. 3. Supplementary feeding prior to laying increased body mass and the level of Igs of females measured at clutch completion. Supplementary fed Ural owl females laid larger eggs than control females, and had offspring with higher levels of Igs at hatching compared to offspring of control females. 4. We found variation in maternal allocation of resources to the eggs in response to environmental conditions: during a year of rapidly declining food abundance, maternal Igs in hatchlings were higher, whereas egg size was smaller compared to years with a more stable food supply. 5. Egg size had a positive effect on offspring body mass at fledging, whereas Igs at hatching did not affect Igs at fledging. 6. We conclude that maternal body condition and maternal Igs, as well as hatchling Igs and egg size are limited by food resources during egg production. Hatchlings rely on maternally derived Igs and, hence, our results suggest that mothers with high levels of Igs passively transfer higher Igs levels to their eggs instead of active manipulation of Igs levels in eggs. Ural owl egg size appears to be highly sensitive to short-term changes in food abundance, with important consequences for nestling growth.

Gender-Related Differences in Nursing Behavior By Roosevelt Elk

Parental investment declines with increasing age of offspring, producing a conflict between parent and offspring over amount of parental investment. The degree of parent-offspring conflict may be associated with the gender of the offspring, mating system such as polygyny, and variation in reproductive success among individuals. We examined the dynamics of maternal investment through time by observing nursing behavior in Roosevelt Elk (Cervus elaphus roosevelti). Suckling rate (P =0.031) and suckling time per bout (P =0.014) by calves decreased with calf age, and male suckling rate (P =0.047) and suckling time per bout (P =0.008) were greater than those for females. Maternal initiation of nursing was greater in the early nursing period (P =0.009), and almost all suckling bouts were terminated by the mother. Our results were similar to those of studies on other polygynous ungulate species which exhibit differences in maternal investment in offspring based on gender.

Mother–offspring associations in Northern muriquis, Brachyteles hypoxanthus

Maternal care of offspring is ubiquitous among primates, but its duration varies across species due to factors such as dispersal patterns and social dynamics, which influence opportunities for and potential benefits of maternal investment in older offspring, respectively. We examined mother-offspring associations in wild northern muriquis (Brachyteles hypoxanthus), in which males are philopatric, females typically disperse before puberty, and social relationships among and between males and females are egalitarian. Associations were systematically recorded between ten mothers, each with two-six offspring in the study group, and all group members from August 2003-May 2004 at the RPPN-Feliciano Miguel Abdala in Minas Gerais, Brazil. Infants of both sexes received similarly high percentages of their mothers' association time. Mothers without infants also maintained strong associations with their youngest juvenile sons. Mothers did not spend consistently more time associating with either juvenile or adult sons than daughters. Our finding of non-preferential associations between muriqui mothers and their older male offspring suggests that extended maternal investment in offspring may be of minimal value in their egalitarian society compared with its value for species living in hierarchical societies.

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.

Genetic Variation in Maternal Investment Patterns in PlatyfishXiphophorus maculatus

Maternal investment in offspring is constrained by a variety of trade-offs, and the investment pattern expressed by an individual can have important fitness consequences. The authors investigate two maternal investment tradeoffs in the southern platyfish, Xiphophorus maculatus: investment in offspring size versus number, and investment in sons versus daughters. Variation in maternal age and size often confound measurements of investment patterns. Because allelic variation at a single locus in platyfish has a major effect on age and size at sexual maturation, investment patterns within a single age and size genotype could be examined, minimizing the influence of these factors on investment patterns. In addition, the platyfish sex determination system allows experimental investigation of relative investment in sons and daughters because different mating types produce different brood sex ratios. Total investment in broods did not differ among sibships, but the investment pattern did; some produced larger but fewer offspring, whereas others produced smaller but more offspring. In addition, there was no evidence of differential investment in sons and daughters; broods with all sons did not differ in size or weight from broods with an equal proportion of the sexes. This result provides direct support for the assumption of equal investment in sons and daughters that is common in discussions of sex-ratio evolution and sex allocation.