Insulin-like growth factor-1 is associated with life-history variation across Mammalia

Despite the diversity of mammalian life histories, persistent patterns of covariation have been identified, such as the ‘fast–slow’ axis of life-history covariation. Smaller species generally exhibit ‘faster’ life histories, developing and reproducing rapidly, but dying young. Hormonal mechanisms with pleiotropic effects may mediate such broad patterns of life-history variation. Insulin-like growth factor 1 (IGF-1) is one such mechanism because heightened IGF-1 activity is related to traits associated with faster life histories, such as increased growth and reproduction, but decreased lifespan. Using comparative methods, we show that among 41 mammalian species, increased plasma IGF-1 concentrations are associated with fast life histories and altricial reproductive patterns. Interspecific path analyses show that the effects of IGF-1 on these broad patterns of life-history variation are through its direct effects on some individual life-history traits (adult body size, growth rate, basal metabolic rate) and through its indirect effects on the remaining life-history traits. Our results suggest that the role of IGF-1 as a mechanism mediating life-history variation is conserved over the evolutionary time period defining mammalian diversification, that hormone–trait linkages can evolve as a unit, and that suites of life-history traits could be adjusted in response to selection through changes in plasma IGF-1.     

The fast-slow continuum in mammalian life history: an empirical reevaluation

Many life-history traits co-vary across species, even when body size differences are controlled for. This phenomenon has led to the concept of a "fast-slow continuum," which has been influential in both empirical and theoretical studies of life-history evolution. We present a comparative analysis of mammalian life histories showing that, for mammals at least, there is not a single fast-slow continuum. Rather, both across and within mammalian clades, the speed of life varies along at least two largely independent axes when body size effects are removed. One axis reflects how species balance offspring size against offspring number, while the other describes the timing of reproductive bouts.     

Hibernation is associated with increased survival and the evolution of slow life histories among mammals

Survival probability is predicted to underlie the evolution of life histories along a slow-fast continuum. Hibernation allows a diverse range of small mammals to exhibit seasonal dormancy, which might increase survival and consequently be associated with relatively slow life histories. We used phylogenetically informed GLS models to test for an effect of hibernation on seasonal and annual survival, and on key attributes of life histories among mammals. Monthly survival was in most cases higher during hibernation compared with the active season, probably because inactivity minimizes predation. Hibernators also have approximately 15 per cent higher annual survival than similar sized non-hibernating species. As predicted, we found an effect of hibernation on the relationships between life history attributes and body mass: small hibernating mammals generally have longer maximum life spans (50% greater for a 50 g species), reproduce at slower rates, mature at older ages and have longer generation times compared with similar-sized non-hibernators. In accordance with evolutionary theories, however, hibernating species do not have longer life spans than non-hibernators with similar survival rates, nor do they have lower reproductive rates than non-hibernators with similar maximum life spans. Thus, our combined results suggest that (i) hibernation is associated with high rates of overwinter and annual survival, and (ii) an increase in survival in hibernating species is linked with the coevolution of traits indicative of relatively slow life histories.     

Does Hibernation Slow the “Pace of Life” in Dwarf Lemurs (Cheirogaleus spp.)?

The classic mammalian life history continuum polarizes small-bodied species that live fast and die young from larger-bodied species with longer life spans and reduced adult mortality rates. Hibernating mammals, however, deviate from this pattern and tend to have short gestations, accelerated early infant growth in preparation for hibernation, retardation of growth and development in association with hibernation, and delayed achievement of full adult size and first reproduction. This pattern has never been systematically tested in hibernating primates. We examine body mass, growth trajectories, dental development, and reproductive status of dwarf lemurs (genus Cheirogaleus), the only obligate hibernators among primates, to determine whether life histories in these small-bodied strepsirrhines vary in accord with expectations based on the use of energy-saving strategies. We show that this pattern does indeed hold for primates. Unlike similarly sized nonhibernating strepsirrhines such as bush babies (genus Galago), wild dwarf lemurs display short gestation and lactation periods, rapid early (pre-hibernation) growth and development followed by retardation of growth and dental development during hibernation, delayed attainment of adult size, and delayed first reproduction. We conclude that hibernation constrains the degree to which dwarf lemurs can experience life in the fast lane. Cheirogaleus have life history profiles that are neither fast nor slow but a combination of both.     

Postnatal allometry of the skeleton in Tupaia glis (Scandentia: Tupaiidae) and Galea musteloides (Rodentia: Caviidae)--a test of the three-segment limb hypothesis

During the evolution of therian mammals, the two-segmented, sprawled tetrapod limbs were transformed into three-segmented limbs in parasagittal zig-zag configuration (three-segment limb hypothesis). As a consequence, the functional correspondence of limb segments has changed (now: scapula to thigh, upper arm to shank, fore arm plus hand to foot). Therefore, the scapula was taken into account in the current study of the postnatal growth of the postcranial skeleton in two small mammalian species (Tupaia glis, Galea musteloides). Comparisons were made between the functionally equivalent elements and not in the traditional way between serially homologous segments. This study presents a test of the three-segment limb hypothesis which predicts a greater ontogenetic congruence in the functionally equivalent elements in fore and hind limbs than in the serially homologous elements. A growth sequence, with decreasing regression coefficients from proximal to distal, was observed in both species under study. This proximo-distal growth sequence is assumed to be ancestral in the ontogeny of eutherian mammals. Different reproductive modes have evolved within eutherian mammals. To test the influence of different life histories on ontogenetic scaling during postnatal growth, one species with altricial juveniles (Tupaia glis) assumed to be the ancestral mode of development for eutherians and one species with derived, precocial young (Galea musteloides) were selected. The growth series covered postnatal development from the first successive steps with a lifted belly to the adult locomotory pattern; thus, functionally equivalent developmental stages were compared. The higher number of allometrically positive or isometrically growing segments in the altricial mammalian species was interpreted as a remnant of the fast growth period in the nest without great locomotor demands, and the clearly negative allometry in nearly all segments in the precocial young was interpreted as a response to the demand on early locomotor activity. Different life histories seem to have a strong influence on postnatal ontogenetic scaling; the effects of the developmental differences are still observable when comparing adults of the two species.     

Plasma prolactin concentrations and cyclic activity in pony mares during parturition and early lactation

Five pony mares were blood sampled during late pregnancy, foaling and early lactation. An homologous assay for horse prolactin was used to measure plasma prolactin concentrations in these samples. Regular estimates of cyclic activity were also made. Plasma prolactin concentrations rose markedly in the last week of pregnancy and remained high although variable in early lactation, before declining to basal levels by 1-2 months post partum. All mares showed a post-partum oestrus 7.0 +/- 0.9 days after parturition. One mare whose foal died shortly after birth showed a rapid decline in plasma prolactin values after death of the foal and an early oestrous period (4 days after parturition). The pattern of prolactin changes reported for the mare are in agreement with those reported for other mammalian species.     

小型啮齿动物的繁殖能量代价

繁殖是动物向后代传递和保持遗传信息的方式。因此繁殖的意义是显而易见的,但也需要付出代价。主要代价是能量需求增加。在对小家鼠繁殖能量需求的研究中发现,能量摄入在妊娠期只是稍微增加,而在哺乳期则急剧增加。尽管在妊娠期增加的幅度很小,但这可能反映了消化道和发育的胎儿之间在动物腹中的空间竞争,从而可能使能量摄入受到限制进而影响到繁殖过程。哺乳期间,能量摄入急剧增加,在哺乳后期达到高峰并趋于稳定。对野生鼠的研究也表明,野生鼠妊娠期和哺乳期的能量摄入模式与小家鼠是基本相同的,这样我们在小家鼠研究工作中的发现就具有更普遍的适应意义。对哺乳后期能量摄入的限制机制研究至少已经进行了15 年。能量摄入受消化道消化能力的限制(中心限制假说)或者受乳腺泌乳能力限制(外周限制假说) 的假说,都不能合理地解释一些现有的结果。我们提出了一个新的假说,即能量摄入可能受啮齿动物散热能力的限制(热耗散限制假说)。很久以来,一直认为散热能力是对大型哺乳动物哺乳的一个限制因素,但它在小型啮齿动物中的意义尚不清楚。传统观点认为,啮齿动物哺乳期对褐色脂肪组织产热水平的调节是为了重新分配能量以满足哺乳所需;但现在看来,实际上可能是动物为了避免体温过高而降低其基本的产热水平。我们在这个领域已经有了一些进展,但要利用这些知识来理解即使很简单的生活史权衡等问题也还有很多的工作需要做。     

Characterization of milk composition in narrow‐ridged finless porpoises (Neophocaena asiaeorientalis) at different lactation stages

Lactation plays a vital role in reproductive success, evolving with ecological adaptations of mammalian life histories. Knowledge of the lactation process in odontocetes is scarce and limited to a handful of species. We investigated the changes in milk composition across different lactation stages, including prepartum mammary secretion and early, mid‐ and late lactation of narrow‐ridged finless porpoises. Prepartum mammary secretion was greenish and characterized by high protein, low sugar, and negligible fat contents. In contrast, milk fat became predominant over protein and sugar contents throughout all lactation stages. At the early lactation stage, the contents of all milk constituents except water varied greatly. At the mid‐late lactation stage, the gross milk composition was relatively stable and was composed of, on average, 67.34% ± 4.13% water, 9.96% ± 0.75% protein, 21.40% ± 3.24% fat, and 1.72% ± 0.73% sugar. Our findings provide new insight into milk composition at different lactation stages in the narrow‐ridged finless porpoise.     

Evolution of age at primiparity in pinnipeds in the absence of the quality–quantity trade‐off in reproduction

Age at primiparity (AP) is a key life history trait which is crucial to the evolution of life history strategies. This trait is particularly interesting in pinnipeds (walrus, eared seals, and true seals), which are monotocous animals. Thus, the commonly observed trade‐off between offspring quality and quantity does not apply to this taxon. Therefore, comparative studies on the evolution of AP might shed light on other important evolutionary correlates when litter size is fixed. Using phylogenetic generalized least squares analyses, we found a strong negative and robust correlation between relative birth mass (mean pup birth mass as a proportion of mean adult female mass) and AP. Rather than trading‐off an early start of reproduction with light relative offspring mass, this result suggests that pinnipeds exhibit either faster (i.e., higher relative offspring mass leading to shorter lactation length, and thus shorter interbirth interval) or slower life histories and that an early AP and a heavy relative offspring mass co‐evolved into a comparatively fast life history strategy. On the other hand, AP was positively related to lactation length: A later start of reproduction was associated with a longer lactation length. Consequently, variation in AP in pinnipeds seems to be affected by an interplay between costs and benefits of early reproduction mediated by relative investment into the single offspring via relative birth mass and lactation length.     

Of mammals and milk: how maternal stress affects nursing offspring

1. A large body of research shows that maternal stress during an offspring’s early life can impact its phenotype in both the short and long term. In the Vertebrata, most research has been focused on maternal stress during the prenatal period. However, the postnatal period is particularly important in mammals because maternal milk provides a conduit by which maternal hormones secreted in response to stressors (glucocorticoids, GCs) can reach offspring. Moreover, lactation outlasts gestation in many species.
2. Though GCs were first detected in milk over 40 years ago, few studies have explored how they affect nursing offspring, and no reviews have been written on how maternal stress affects nursing offspring in the natural world.
3. We discuss the evolution of milk and highlight its importance in each of the three mammalian lineages: monotremes (subclass Monotremata), marsupials (infraclass Marsupialia), and eutherians (infraclass Placentalia). Most research on the effects of milk GCs on offspring has been focused on eutherians, but monotremes and marsupials rely on their mothers’ milk for a proportionally longer period of time, and so research on these taxa may yield more insight.
4. We show that GCs are important for milk production, both during an individual nursing bout and over the entire lactation period, and review evidence of GCs moving from maternal blood to milk, and eventually to nursing offspring. We examine evidence from rodents and primates of associations between GC levels in lactating females (either blood or milk) and offspring behaviour and growth rates. We discuss ways that maternal stress may impact these offspring phenotypes outside of milk GCs, such as changes to: (1) milk output, (2) other milk constituents (e.g. macronutrients, growth factors, cytokines), and (3) maternal care behaviour.
5. Critical to understanding the fitness impacts of elevated maternal GC levels during lactation is to place this within the context of the natural environment. Species-specific traits and natural histories will help us to understand why such maternal stress produces different offspring phenotypes that equip them to cope with and succeed in the environment they are about to enter.

     

Trans-Generational Effect of Maternal Lactation during Pregnancy: A Holstein Cow Model

Epigenetic regulation in mammals begins in the first stages of embryogenesis. This prenatal programming determines, in part, phenotype expression in adult life. Some species, particularly dairy cattle, are conceived during the maternal lactation, which is a period of large energy and nutrient needs. Under these circumstances, embryo and fetal development compete for nutrients with the mammary gland, which may affect prenatal programming and predetermine phenotype at adulthood. Data from a specialized dairy breed were used to determine the transgenerational effect when embryo development coincides with maternal lactation. Longitudinal phenotypic data for milk yield (kg), ratio of fat-protein content in milk during first lactation, and lifespan (d) from 40,065 cows were adjusted for environmental and genetic effects using a Bayesian framework. Then, the effect of different maternal circumstances was determined on the residuals. The maternal-related circumstances were 1) presence of lactation, 2) maternal milk yield level, and 3) occurrence of mastitis during embryogenesis. Females born to mothers that were lactating while pregnant produced 52 kg (MonteCarlo standard error; MCs.e. = 0.009) less milk, lived 16 d (MCs.e. = 0.002) shorter and were metabolically less efficient (+0.42% milk fat/protein ratio; MCs.e.<0.001) than females whose fetal life developed in the absence of maternal lactation. The greater the maternal milk yield during embryogenesis, the larger the negative effects of prenatal programming, precluding the offspring born to the most productive cows to fully express their potential additive genetic merit during their adult life. Our data provide substantial evidence of transgenerational effect when pregnancy and lactation coincide. Although this effect is relatively low, it should not be ignored when formulating rations for lactating and pregnant cows. Furthermore, breeding, replacement, and management strategies should also take into account whether the individuals were conceived during maternal lactation because, otherwise, their performance may deviate from what it could be expected.     

Effects of life history variation on vertical transfer of toxicants in marine mammals

Toxicant bioaccumulation poses a risk to many marine mammal populations. Although individual-level toxicology has been the subject of considerable research in several species, we lack a theoretical framework to generalize the results across environments and life histories. Here we formulate a dynamic energy budget model to predict the effects of intra- and interspecific life history variation on toxicant dynamics in marine mammals. Dynamic energy budget theory attempts to describe the most general processes of energy acquisition and utilization in heterotrophs. We tailor the basic model to represent the marine mammal reproductive cycle, and we add a model of toxicant uptake and partitioning to describe vertical transfer of toxicants from mother to offspring during gestation and lactation. We first show that the model predictions are consistent with qualitative patterns reported in empirical studies and previous species-specific modeling studies. Next, we use this model to examine the dependence of offspring toxicant load on birth order, food density, and interspecific life history variation.     

Maternal Effort is State Dependent: Energetic Limitation or Regulation?

Many small altricial rodents have a postpartum oestrus and are often simultaneously pregnant and lactating. Negative influences of concurrent pregnancy and lactation on both lactational performance and the litter in utero are commonly observed and have been interpreted as resulting from high simultaneous energetic demands of gestation and lactation. We studied these effects in the precocial guinea‐pig (Cavia aperea f. porcellus) that, like many altricial rodents, has a postpartum oestrus, but in which the peaks of energy expenditure on lactation and gestation are widely separated. This life history allowed to investigate whether physiological regulation other than by energetic limitations may be responsible for allocation conflicts arising when lactation and gestation overlap. By comparing simultaneously pregnant and lactating females with lactating non‐pregnant females, we show that females in the former group nurse less and wean earlier than females of the latter group. In a comparison of litter size, litter mass, and pup mortality of females that had not been lactating during pregnancy with females that had been simultaneously pregnant and lactating, we show that the latter do not reduce investment in the following litter. In our study, energetic constraints on ad libitum fed females are unlikely and we therefore suggest that the results must be explained by regulatory constraints on lactational effort. We point out that this explanation has not been excluded for the effects observed in altricial small mammals.     

Ecology and evolution of mammalian biodiversity

Mammals have incredible biological diversity, showing extreme flexibility in eco-morphology, physiology, life history and behaviour across their evolutionary history. Undoubtedly, mammals play an important role in ecosystems by providing essential services such as regulating insect populations, seed dispersal and pollination and act as indicators of general ecosystem health. However, the macroecological and macroevolutionary processes underpinning past and present biodiversity patterns are only beginning to be explored on a global scale. It is also particularly important, in the face of the global extinction crisis, to understand these processes in order to be able to use this knowledge to prevent future biodiversity loss and loss of ecosystem services. Unfortunately, efforts to understand mammalian biodiversity have been hampered by a lack of data. New data compilations on current species' distributions, ecologies and evolutionary histories now allow an integrated approach to understand this biodiversity. We review and synthesize these new studies, exploring the past and present ecology and evolution of mammalian biodiversity, and use these findings to speculate about the mammals of our future.     

A study of some serum mineral levels before and during pregnancy and during lactation period of sheep and cattle

The purpose of this study was to determine serum Cu, Zn, Mn, K, and Mg levels before and during pregnancy and during the lactation period of sheep and cattle and to determine the relationships between periods. For this purpose, blood samples of 14 healthy, pregnant Brown Swiss cows fed under normal condition and 36 Karakaş (İvesi × Akkaraman) sheep were used. Blood samples were analyzed using an atomic absorption spectrophotometer. There were significant differences between before pregnancy and during pregnancy, and during pregnancy and the lactation period for serum Zn concentration; also before pregnancy and during pregnancy, and before pregnancy and the lactation period for serum K concentration in cows (p<0.05). There were significant differences between before pregnancy and the lactation period for serum Cu concentration, and before pregnancy and during pregnancy for serum K concentration; also pregnancy and the lactation period for serum Mg concentration in sheep (p<0.05).     

Aping our ancestors: Comparative aspects of reproductive ecology

There are many similarities among mammalian species in how ecological factors affect their reproductive potential and individual life histories. One of the most important limiting factors is the availability of sufficient resources to partition among essential growth, maintenance, and eventual reproduction.^1–3 How each mammal juggles these constraints constitutes its unique life history and determines its success as a species. Yet, as Hill and Hurtado⁴ recently argued, life-history analyses are rarely applied to human reproduction. In fact, despite the demonstrated significance of adequate nutrition for reproductive performance among most mammalian species that have been studied,^1,3,5 many demographers, and even some biological anthropologists, have resisted the idea that humans, except under extreme famine conditions, might be subject to the same kinds of nutritional constraints that affect other mammals.^6–9.     

Concurrent lactation and pregnancy: pregnant domestic horse mares do not increase mother-offspring conflict during intensive lactation

Lactation is the most energy demanding part of parental care in mammals, so parent-offspring conflict arises over milk provided by the mother. In some species females commonly become pregnant shortly after parturition of previous young. This further intensifies mother-offspring conflict due to concurrent pregnancy and lactation. In equids it has been well established that pregnant females wean their foals earlier than non-pregnant ones. Intensified mother-offspring conflict was presumed to associate with pregnancy also during the period of intensive lactation, i.e., before the weaning process starts. We investigated the effect of pregnancy on suckling behaviour characteristics as indicators of mother-offspring conflict in domestic horses. Contrary to expectation, here we provide evidence of a decreased mother-offspring conflict related to pregnancy in lactating females during first two trimesters of pregnancy. Pregnant mares provided longer suckling bouts and did not reject or terminate suckling of their foals more often than non-pregnant mares. Our results suggest that pregnant mares cope with parallel investment into a nursed foal and a foetus through enhancing nursing behaviour in early stages of pregnancy before the initially low requirements of the foetus increase. They compensate their suckling foal with the perspective of its early weaning due to ongoing pregnancy.     

Effect of mother’s physical condition during pregnancy and lactation on postnatal growth and reproductive success of offspring in water vole <Emphasis Type="Italic">Arvicola terrestris</Emphasis>

Postnatal growth, life span, and probability of reproduction in the adult state depended on the mother’s physical condition during pregnancy and lactation in water vole. The white fat weight in the female abdominal cavity was shown to significantly increase in pregnancy and to decrease in late lactation. As an indicators for nutritional state of females, their body weight difference after parturition (or in late lactation) and expected from the regression equation relating individual body weight at the beginning and the end of each reproductive stage were used (physical condition indexes in pregnancy or lactation). The correlation of the physical condition index in pregnancy with the storage fat weight was 0.67. The metabolic resources of the mother’s body proved to favor faster offspring development. The female offspring weight at the age of 3 and 10 weeks as well as adult ones positively correlated with the mother’s nutritional state in pregnancy, while the male offspring weight demonstrated a similar correlation at the age of 3 and 6 weeks. Increased negative energy balance during lactation proved to decrease the offspring weight in both sexes after separation from mother and at the age of 6 weeks. High nutritional state of mother in pregnancy favored both the probability of reproduction and life span of female offspring. The reproduction of male offspring did not depend on the mother’s physical condition. The life span peaked in male offspring of mothers in a nutritional state below average in pregnancy and above average in lactation. Thus, the physical condition of the mother’s body is an important sex-dependent factor of phenotypic variation in the offspring body weight, reproductive competence, and life span.     

Maternal food restriction delays weaning in the guinea pig, Cavia porcellus

In mammals, the duration of lactation varies much more than other life history parameters in relation to body mass, both within and between species. The causes of this variation are poorly understood and seem to result from varying conditions of mothers and young. We studied the effect of long-term maternal food restriction on litter mass at birth, duration of lactation and offspring development in the precocial guinea pig. Mild experimental food restriction during reproduction resulted in prolonged nursing behaviour of mothers. Evidence for a threshold mass at weaning was, however, equivocal. In the guinea pig, benefits of prolonged lactation prove hard to understand, because nutritional benefits are minor. Independently of maternal food regime, pups terminated suckling attempts several days after mothers ceased nursing behaviour. The time between the last nursing behaviour and the last suckling attempts was not longer in litters with higher need, that is, in litters of food-restricted females, than in litters of females fed ad libitum. Under food restriction, mothers maintained their own body mass, leading in pups to lower mass at birth, reduced postnatal growth and lower body mass at maturity. Guinea pig mothers appear to be selected to value their own condition more than that of a litter. We suggest that lengthening of the nursing period under poor conditions is a life history response primarily of precocial mammals.