The influence of birth timing upon infant growth and survival in Captive Rhesus Macaques (Macaca mulatto)

Weights, growth rates, and mortality data of 815 captive-born Macaca mulattainfants were studied to determine if date of birth influences infant growth and survival. The six groups studied displayed a unimodal spring-summer birth season that has become systematically more restricted since 1977. Males exhibited higher rates of stillbirth and neonatal death and were more frequently born outside the normal birth season, when infant mortality was more common. Within the normal birth season, infant weight increased linearly with birth date, and infant growth rate declined linearly with birth date. Female infants with weights and growth rates near the developmental norm, especially those born in the middle of the birth season, have the greatest probability of survival. Males are more likely to survive if their weights and growth rates exceed the developmental norm, and thus male infants might be initially more costly to produce than female infants. These results are inconsistent with the hypothesis that offspring of high-ranking males, which conceived predominantly in the first third of the breeding season, enjoy a selective advantage.     

Growth and developmental outcomes of three high-risk infant rhesus macaques (Macaca mulatta)

Infants classified as "high risk" are born with a greater chance of developing medical complications at birth, and may have cognitive and other developmental complications later in life. Very few reports exist regarding the survival and outcome of such infants in primate colonies. Here we present early growth and developmental data on three high-risk infant rhesus macaques (one female and two males) that were born either with intrauterine growth restriction (IUGR; born below the 1st birth weight percentile for gestational age) or extremely prematurely (at gestational days 128 and 140; mean full-term gestation=164 days). We compared the outcome of these infants with that of healthy controls born at term and found no gross developmental delays in these infants with respect to growth, neonatal reflex and motor skill development, early cognitive development, or social behavior. Neurological and cognitive assessments were compared in terms of both postnatal and gestational age. The survival of these infants was dependent on a 24-hr staffed nursery and a fluid protocol that catered to each high-risk infant's individual needs. When such measures are implemented, infants such as these have a good chance of survival and can serve as excellent models for high-risk human babies and their subsequent development.     

Animal learning as a source of developmental bias

As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path‐dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution.     

A descriptive analysis of gut microbiota composition in differentially reared infant rhesus monkeys (Macaca mulatta) across the first 6 months of life

The gastrointestinal microbiome is recognized as a critical component in host immune function, physiology, and behavior. Early life experiences that alter diet and social contact also influence these outcomes. Despite the growing number of studies in this area, no studies to date have examined the contribution of early life experiences on the gut microbiome in infants across development. Such studies are important for understanding the biological and environmental factors that contribute to optimal gut microbial colonization and subsequent health. We studied infant rhesus monkeys (Macaca mulatta) across the first 6 months of life that were pseudo‐randomly assigned to one of two different rearing conditions at birth: mother‐peer‐reared (MPR), in which infants were reared in social groups with many other adults and peers and nursed on their mothers, or nursery‐reared (NR), in which infants were reared by human caregivers, fed formula, and given daily social contact with peers. We analyzed the microbiome from rectal swabs (total N = 97; MPR = 43, NR = 54) taken on the day of birth and at postnatal Days 14, 30, 90, and 180 using 16S rRNA gene sequencing. Bacterial composition differences were evident as early as 14 days, with MPR infants exhibiting a lower abundance of Bifidobacterium and a higher abundance of Bacteroides than NR infants. The most marked differences were observed at 90 days, when Bifidobacterium, Lactobacillus, Streptococcus, Bacteroides, Clostridium, and Prevotella differed across rearing groups. By Day 180, no differences in the relative abundances of the bacteria of interest were observed. These novel findings in developing primate neonates indicate that the early social environment as well as diet influence gut microbiota composition very early in life. These results also lay the groundwork for mechanistic studies examining the effects of early experiences on gut microbiota across development with the ultimate goal of understanding the clinical significance of developmental changes.     

Environmental influences on the evolution of growth and developmental rates in passerines

Abstract.— The reasons why growth and developmental rates vary widely among species have remained unclear. Previous examinations of possible environmental influences on growth rates of birds yielded few correlations, leading to suggestions that young may be growing at maximum rates allowed within physiological constraints. However, estimations of growth rates can be confounded by variation in relative developmental stage at fledging. Here, we re-estimate growth rates to control for developmental stage. We used these data to examine the potential covariation of growth and development with environmental variation across a sample of 115 North American passerines. Contrary to previous results, we found that growth rates of altricial nestlings were strongly positively correlated to daily nest predation rates, even after controlling for adult body mass and phylogeny. In addition, nestlings of species under stronger predation pressure remained in the nest for a shorter period, and they left the nest at lower body mass relative to adult body mass. Thus, nestlings both grew faster and left the nest at an earlier developmental stage in species with higher risk of predation. Growth patterns were also related to food, clutch size, and latitude. These results support a view that growth and developmental rates of altricial nestlings are strongly influenced by the environmental conditions experienced by species, and they generally lend support to an adaptive view of interspecific variation in growth and developmental rates.     

Ecological correlates to social structure in two lemur species in Madagascar

In this study, I tested two hypotheses regarding the relationship of ecological variables (size, density, and distribution of patches) and infant developmental patterns to lemur social structure using two prosimian primates in Ranomafana, Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Three predictions regarding the general effects of patch size and subgroup size on lemur feeding rates were supported: (1) Rufous lemurs used large patches; red-bellied lemurs used smaller patches; (2) larger subgroups of rufous lemurs used larger patches; and (3) rufous lemur feeding rates decreased significantly with increases in subgroup size and patch size, whereas size and patch size had no significant effect on red-bellied lemur feeding rates. However, food item size (fruit) had a more significant effect on rufous and red-bellied lemur feeding rates than either patch size or subgroup size. When similar-sized fruits were compared, rufous lemur feeding rates on small fruit were most affected by patch size, yet feeding rates on medium-sized fruit were most affected by subgroup size. Neither lemur species used patches in consistent ways seasonally. During periods of food abundance, rufous lemurs used many small, common, and clumped patches. In food scarcity periods, they used fewer, larger, rarer, and less clumped patches; groups migrated when food became most scarce. Red-bellied lemurs also used patches in variable ways, but these patterns were not linked with food availability. Finally, infant development patterns differed between lemur species; red-bellied lemur males cared for offspring and infants reached developmental landmarks faster than rufous lemur infants. Therefore, red-bellied lemur group size may be constrained by the need for additional infant care by other group members. In contrast, rufous lemur group size may be constrained by patch availability during the most critical period of food scarcity. © 1996 Wiley-Liss, Inc.     

Life history divergence of sympatric diploid and polyploid populations of brine shrimp Artemia parthenogenetica

In order to study how polyploidy affects life history patterns in animals, we have examined sympatric diploid and polyploid brine shrimp (Artemia parthenogenetica) from China, Italy and Spain under laboratory conditions. At optimal temperature and salinity (25°C and 90 ppt), diploids from the three populations had much higher intrinsic rates of increase, higher fecundity, faster developmental rates, and larger brood sizes than their sympatric polyploids. The Chinese and Italian populations were selected for further analysis to determine the life history responses of diploids and polyploids to temperature and salinity changes. Under intermediate and high salinities, Chinese and Italian polyploids produced most of their offspring as dormant cysts while their sympatric diploids produced most of their offspring as nauplii. This relationship is reversed in the Spanish diploid-polyploid complex. For the Chinese population at 25° C, pentaploid clones had higher developmental rates than diploid clones at 35 ppt; at 90 ppt, diploid clones had higher developmental rates than the pentaploids. Italian diploids and tetraploids had different responses to variation in both temperature (25° C and 31° C) and salinity (30 ppt and 180 ppt). Our results demonstrate that relative fitness of the two cytotypes is a function of environmental conditions and that sympatric diploids and polyploids respond differently to environmental changes. Chinese and Italian polyploids are expected to have lower fitness than their sympatric diploids when the physical environment is not stressful and when intraspecific competition is important. However, polyploids may have advantages over sympatric diploids in stressful habitats or when they encounter short-term lethal temperatures. These results suggest that polyploid Artemia have evolved a suite of life-history characteristics adapting them to environments that contrast to those of their sympatric diploids.     

Development and mother-infant relations among captive patas monkeys

Generalizations about the rate of behavioral development and mother-infant relations in nonhuman primates are often based largely on observations of a few closely related species of macaques. Patas monkeys (Erythrocebus patas)are sufficiently distant phylogenetically and distinct in their social and ecological adaptations from the well-studied macaque species that observations of their patterns of infant development and mother-infant relations may indicate to what extent macaque patterns are typical of Old World monkey species. Eight patas infants living with their mothers in an established captive group were observed for 960 hr over the first year of life. These infants showed a rapid rate of behavioral development and attainment of independence from mothers. Patas also have one of the fastest rates of sexual maturation of any Old World monkey species. This pattern of rapid social and sexual development can be viewed as a response to a highly seasonal savannah environment in which there is a premium on ability to achieve nutritional, locomotor, and social self-sufficiency as quickly as possible and to reproduce as early and as often as developmental constraints will permit. Patterns of infant development and mother-infant relations may be best understood as an integral part of a species’ overall life history pattern.     

巨大儿与足月适于胎龄儿2 岁以内的体格及智能发育的对照研究

目的：了解出生体重对婴儿早期体格及智能发育的影响,为巨大儿的早期保健及健康教育提供理论依据。方法：在我院2007 年1 月～2009 年12 月出生的巨大儿及足月适于胎龄儿中,随机选取50 例足月巨大儿作为观察组(除外生后低血糖、窒息、高胆 红素血症者),及50 例与之匹配的足月适于胎龄儿作为对照组。两组孕周、生后评分、性别比例、父母收入、喂养方式比较差异无统 计学意义。定期检查和记录两组的各体格及智能发育评估指标,了解两组婴儿体重指数及智能发育特点,采用Gesell发育诊断量 表对两组进行评价。结果：观察组出生后3、6、9、12、18、24 个月的超重发生率均显著高于对照组,差异均有统计学意义(P<0.05), 观察组随年龄增长体重指数有下降趋势,6 月龄时体重指数最高,24 月时最低;观察组6 月时大运动发育商数为(100.86± 3.34), 对照组则为(104.58± 3.19),差异有统计学意义(P<0.05),12 月时,观察组的发育商数已接近正常,两组大运动、精细运动、适应行 为、语言和个人- 社会性行为5 个方面的的差异均无统计学意义(P>0.05)。结论：巨大儿在2 岁以内的体重指数显著高于足月适于 胎龄儿;较重的体重负荷可对其生后6 月内的大运动造成不良影响。     

Physical Environmental Effects on Infant Care and Development in Captive Callithrix jacchus

Environmental enrichment may affect infant care and development in captive primates. We investigated the effects of this factor in laboratory common marmosets (Callithrix jacchus). An enriched physical environment enhanced the social activities of the marmosets and elicited a greater repertoire of behaviors, without negatively affecting the provision of infant care. In addition, infants in enriched cages displayed certain behaviors sooner than infants in non-enriched cages did, which suggests an increased developmental rate. Infants in enriched cages also ate more solid food and engaged in solitary play and exploration more than ones in non-enriched cages did. Play and exploration probably improve spatial cognition and motor skills, which, together with a higher degree of independence, may allow infants to cope better with laboratory routines and general social interactions later in life than their counterparts reared in less complex enclosures. We conclude that laboratories can significantly increase the welfare of marmosets by providing a more complex physical environment.     

Selective interactions among Rh,ABO, and sex ratio of newborns

Summary The hypothesis that the Rh and ABO blood systems behave like the HLA system in relation to mother-conception tolerance-rejection mechanisms was tested in 25,501 mother-infant pairs. According to this hypothesis, heterozygotes carrying a paternal gene that is not present in their mother should be better tolerated than homozygotes. Significantly more BO infants born to AO mothers. AO infants born to BO mothers, Rh(+) heterozygotes born to Rh(-) mothers, and less significantly AO infants born to OO mothers confirm the hypothesis. Fewer homozygotes occurred in Rh(-) infants born to Rh(+) mothers and in O infants born to non-O mothers. Deviations from the Hardy-Weinberg equilibrium found in the ABO system were modified by the Rh and sex of the infant. These data strongly support the hypothesis that at least two feto-maternal systems influence the denstiny of pregnancies: the classical known incompatibility system which operates late in pregnancy and a new one which is based on the induction of maternal tolerance early in pregnancy: maternal tolerance seems to be better elicited by heterozygous eggs or embryos carrying a gene not present in the mother. The data also support the hypothesis that the sex ratio is influenced by feto-maternal tolerance-rejection mechanisms associated with the ABO and Rh systems.     

The roles of pre‐ and post‐hatching growth rates in generating a latitudinal cline of body size in the eastern fence lizard (Sceloporus undulatus)

Countergradient variation in norms of reaction can dampen the direct effects of environmental influences on phenotypic traits, allowing phenotypic similarity among populations despite exposure to different environmental conditions. Such norms of reaction may occur at any phase of the life‐history (e.g. growth rates during both embryonic and postembryonic stages may influence geographical variation in adult body size). We collected gravid female lizards (Sceloporus undulatus) from northern (Indiana), central (Mississippi), and southern (Florida) populations, spanning almost the full latitudinal range of the species. Adult females from the southern population were smaller. Intrinsic growth rates of hatchlings were higher for the central population than for the other two populations. This pattern does not parallel the countergradient variation previously found in embryonic developmental rates among these populations. Earlier hatching enhanced survival rates of juveniles to a similar degree among populations, although juvenile survival rates in the field generally increase with latitude in this species. Our data reveal geographical variation in the ways in which intrinsic developmental/growth rates and survival shift during ontogeny, and suggest that latitudinal patterns in adult body size (such as Bergmann's rule) can result from both faster growth, and longer periods of growth. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 202–209.     

Zur Funktion von Warnfarben: Die Reaktion junger Stare auf wespenähnlich schwarz-gelbe Attrappen

Social regulation of developmental rate of the African cichlid fish, Haplochromis bur-toni, was studied experimentally. Broods were raised under three different social conditions: total isolation, with no visual, physical or chemical contact with siblings; physical isolation, with no physical or chemical contact with siblings; and in social groups. Development of behavior and color patterns were observed in fish from 2 to 14 weeks of age. Males were sacrificed at 4-week intervals to measure growth and maturation state. Results showed that developmental rate is influenced by the social environment. Males with no territories (raised in groups) grew and matured more slowly than those in all other conditions. These males were not prevented from maturing but both the rate and phenotypic expression of maturation were inhibited.     

HETEROZYGOSITY AND DEVELOPMENTAL RATE IN A STRAIN OF RAINBOW TROUT (SALMO GAIRDNERI)

Rainbow trout (Salmo gairdneri) with greater heterozygosity at enzyme loci also have greater developmental stability, as measured by bilateral symmetry of five meristic traits. Fish with increased amounts of liver phosphoglucomutase activity have greater developmental stability and develop faster than fish with normal activity. These observations suggest that the differences in developmental stability between homozygotes and heterozygotes may be the result of differences in developmental rate. Faster developmental rates are expected to decrease the probability of accidents during critical periods of development, resulting in a more stable or uniform phenotype. As indicated by differences in hatching time, heterozygotes tend to develop more rapidly than homozygotes. This association is not strongly expressed within families at any locus except Pgm1-t. However, heterozygotes for Mdh3,4 and Hex hatched significantly sooner than homozygotes in a population sample. These results suggest that differences in developmental rate between homozygotes and heterozygotes may account for the positive association between developmental stability and heterozygosity in rainbow trout.     

巨大儿与足月适于胎龄儿2岁以内的体格及智能发育的对照研究

目的：了解出生体重对婴儿早期体格及智能发育的影响,为巨大儿的早期保健及健康教育提供理论依据。方法：在我院2007年1月～2009年12月出生的巨大儿及足月适于胎龄儿中,随机选取50例足月巨大儿作为观察组（除外生后低血糖、窒息、高胆红素血症者）,及50例与之匹配的足月适于胎龄儿作为对照组。两组孕周、生后评分、性别比例、父母收入、喂养方式比较差异无统计学意义。定期检查和记录两组的各体格及智能发育评估指标,了解两组婴儿体重指数及智能发育特点,采用Gesell发育诊断量表对两组进行评价。结果：观察组出生后3、6、9、12、18、24个月的超重发生率均显著高于对照组,差异均有统计学意义（P〈0.05）,观察组随年龄增长体重指数有下降趋势,6月龄时体重指数最高,24月时最低;观察组6月时大运动发育商数为（100.86±3.34）,对照组则为（104.58±3.19）,差异有统计学意义（P〈0.05）,12月时,观察组的发育商数已接近正常,两组大运动、精细运动、适应行为、语言和个人-社会性行为5个方面的的差异均无统计学意义（P〉0.05）。结论：巨大儿在2岁以内的体重指数显著高于足月适于胎龄儿;较重的体重负荷可对其生后6月内的大运动造成不良影响。     

Isolation of females prior to parturition reduces neonatal mortality in Galago

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effects of isolation of pregnant females on neonatal mortality rates. Isolation significantly decreased neonatal mortality rates in all three species over neonatal mortality rates in infants born to unisolated females. The frequency of cannibalism of infants did not differ between isolated and unisolated females. Secondary sex ratio differed significantly from 1:1 for all three species, but higher mortality in males in the first 10 days of life resulted in sex ratios that did not differ from 1:1 in G. garnettii and G. crassicaudatus.     

Variations in care for cottontop tamarin, Saguinus oedipus, infants as a function of parental experience and group size

We examined the effects of parental experience and group size on infant care and development. Ten cottontop tamarin families were followed across three consecutive births of offspring to examine differences in survival, quality of care, developmental maturation and physical development for infants in two experimental conditions: (1) in large groups with previous parenting experience and (2) in small groups with little or no parenting experience. Although we found no differences in infant mortality, parents treated infants differently between conditions. However, when we examined the cumulative care provided by parents and sibling helpers together across experimental conditions, there were no differences in the rates of retrieval or rejection of infants. Overall levels of infant transport and food transfers were similar between conditions, with fathers and sibling helpers contributing the bulk of care. Fathers in small groups carried infants and transferred food with infants much more than helpers but, as group size increased, helpers augmented this role. Infant development varied with the experience of the family both between conditions and within a family. The results indicate that infants receive similar levels of care regardless of group size and parenting experience, although the individual contributions of family members change with both factors. Parental experience with previous infants had effects on early infant development, but only for the first sets of infants. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Sex Ratio Adjustment in a Seasonally Breeding Primate Species: Evidence from the Barbary Macaque Population at Affenberg Salem

Presented are data on secondary sex ratio in a large population of semifree-ranging Barbary macaques (Macaca sylvanus) at Affenberg Salem. Examined were 569 births in five social groups with regard to demographic parameters, maternal age and rank. Significant differences were found between the secondary sex ratios of high ranking and low ranking females. A higher proportion of male offspring was born in the high ranking class, while both groups did not differ in fecundity rates. A detailed analysis of the reproductive cycles of 73 females showed a significant shorter interval between the end of conceptional estrus and birth in male infants and also a significantly earlier onset of deturgescence of anogenital swelling when males were conceived. These results strongly suggest that the differences in the secondary sex ratio are not due to differential abortions but rather to pre-conceptional control of sex via timing of mating in relation to ovulation.     

Male rank,reproductive behavior,and reproductive success in free-ranging rhesus macaques

Paternity assessment through DNA fingerprinting by synthetic oligonucleotide probes was applied to one birth cohort in a social group of free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago. The 11 group males and 9 males from other groups were observed mating with the females. Paternity was determined for 11 of the 15 infants. Male dominance rank was not associated with reproductive success. High-ranking resident males (N=5) sired 27% of the infants born during a one-year study. Four of the 11 infants of known paternity were sired by males of other social groups. The four infants of unknown paternity were sired either by males not observed mating with the females or the low-ranking male who was not fingerprinted. Male dominance rank was not associated with reproductive activity during conception cycles. These results suggest that the effect of rank on male reproductive success is not a predictable correlation, but a conditional probability.     

Egg environments have large effects on embryonic development,but have minimal consequences for hatchling phenotypes in an invasive lizard

Plastic responses of embryos to developmental environments can shape phenotypes in ways that impact fitness. The mechanisms by which developmental conditions affect offspring phenotypes vary substantially among taxa and are poorly understood in most systems. In this study, we evaluate the effects of thermal and hydric conditions on patterns of egg water uptake, embryonic development and yolk metabolism in embryos of the lizard Anolis sagrei to gain insights into how these factors shape morphological variation in hatchlings. Our 3 × 2 experimental design (3 thermal and 2 hydric conditions) revealed that developmental temperature has strong effects on rates of development and yolk metabolism, but the impacts of moisture were minimal. Increased water uptake by eggs under relatively wet conditions resulted in larger hatchlings with less internalized residual yolk than hatchlings from dry‐incubated eggs. However, the relatively small phenotypic differences among treatments may have small fitness consequences. These results demonstrate that embryos of A. sagrei can tolerate a broad range of environmental conditions without substantial impacts on critical morphological traits. Such embryonic tolerances may facilitate colonization and establishment in novel environments. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 25–41.