Effects of macroparasites on the energy allocation of reproducing small mammals

Reproduction, including lactation, is the most costly activity in terms of energy expenditure in female mammals. Consequently, the energy requirements of the reproducing female may not be met at this time, especially if other energy demanding activities are occurring concomitantly. Such activities could be the activation and maintenance of an immune system in response to parasitic infestation. These protective processes are energetically demanding and require trade-off decisions among competing energy demands. In the case of a reproducing mammal, the trade-offs occur mainly between defence against parasites and reproductive costs of the host. In this paper, I discuss the effects of macroparasites on the energy allocation of reproducing small mammals.     

Reproductive energetics of the nectar-feeding bat<Emphasis Type="Italic"> Glossophaga soricina</Emphasis> (Phyllostomidae)

Pregnancy and lactation are energetically demanding periods for female mammals. Unique amongst mammals, bats have to allocate considerable amounts of energy into their offspring because juveniles cannot be weaned until they are capable of flying at almost adult size. Similar to other bat species, female nectar-feeding bats should increase their energy intake after parturition to meet the energy demands of offspring growth. However, previous studies have shown that nectar-feeding bats differ from other similar-sized bats in having a much higher metabolic rate. Therefore, I examined how nectarivorous bats respond to the energetic challenge of reproduction. In this study, the daily energy intake of pregnant and lactating Glossophaga soricina was measured during a 6-week period prior to and a 10-week period after parturition. Body mass of G. soricina increased linearly until parturition. Within the same time period, daily flight time decreased and daily energy intake remained constant. Probably, the reduced flight activity of pregnant bats compensated for the increased power requirements of flight, thus resulting in an almost constant daily energy turnover. During 35 days after parturition, neither flight time, body mass nor daily energy intake of lactating females changed significantly. On average, the daily energy intake of pregnant, lactating or non-reproducing G. soricina was not significantly different. Possibly, for unknown reasons, female G. soricina maintain a daily energy intake of a constant high level during and beyond reproduction.     

Effects of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra)

Lactation is an energy demanding phase in the reproductive cycle of female mammals. For this reason, several studies have assessed the effects of lactation on female behavior. In this study we examine the influence of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra) in Campeche, Mexico. We observed 32 adult females and 35 infants belonging to 14 groups of black howlers for a total of 2,224 focal hours. We found that lactating females spent more time being inactive and feeding from fruits than nonlactating females. In addition, during the first two-thirds of lactation females were more active (i.e., rested less, fed more, devoted more time to social activities, and moved more) and foraged more intensively (i.e., ranged over larger distances, used more feeding trees and feeding species, and consumed more leaves) than females in the last third of lactation. Lactation seems to force black howler females to reduce activity and to maximize the intake of high-quality foods, with inactivity being the highest during late lactation, when females probably face the cumulative effects of nursing older infants and of a new pregnancy. Early lactation is probably the most energetically demanding stage of lactation for black howler females. This study demonstrates that despite being energetically constrained by a highly folivorous diet, reproductive state affects several dimensions of the behavior of black howler females. Therefore, variation in time-budgets and foraging strategies of howlers has been probably underestimated by previous research that has not considered physiological differences among individuals.     

The effects of intracranial implantation of estrogen on receptivity in sexually and asexually reproducing female whiptail lizards, Cnemidophorus inornatus and Cnemidophorus uniparens

The ventromedial hypothalamus (VMH) is an important site in the neuroendocrine control of sexual receptivity in mammals. This study was conducted to determine if the VMH was also involved in estrogen induction of receptivity in whiptail lizards. Estradiol benzoate (EB) was implanted into the VMH of ovariectomized Cnemidophorus inornatus, a sexually reproducing species, and C. uniparens, a parthenogenetic species which displays "pseudosexual" behaviors similar to the sexual behaviors typical of both male and female C. inornatus. In both species, EB was significantly more effective in eliciting receptivity when implanted in the VMH than in other locations in the brain. These results support the idea that, as in mammals, the VMH is an important location of estrogen action in the control of receptive behaviors in both sexually and asexually reproducing whiptail lizards.     

Variable variation: annual and seasonal changes in offspring sex ratio in a bat

Many organisms produce offspring with sex-ratios that deviate from equal numbers of males and females, and numerous adaptive explanations have been proposed. In some species, offspring sex-ratio varies across the reproductive season, again with several explanations as to why this might be adaptive. However, patterns for birds and mammals are inconsistent, and multiple factors are likely involved. Long-term studies on a variety of species may help untangle the complexity. I analyzed a long-term data set on the variation in offspring sex-ratio of the big brown bat, Eptesicus fuscus, a temperate-zone, insectivorous species. Sex ratio varied seasonally, but only in some years. Births early in the season were significantly female biased in years in which parturition occurred relatively early, but not in years with late parturition. Survival of female pups increased with earlier median birth date for the colony, and early-born females were more likely to survive and reproduce as one-year olds, compared to later-born pups. I argue that, due to the unusual timing of reproductive activities in male and female bats that hibernate, producing female offspring early in the year increases their probability of reproducing as one year olds, but this is not the case for male offspring. Thus, mothers that can give birth early in the year, benefit most by producing a female pup. The relative benefit of producing female or male offspring varies depending on the length of the growing season and thus the time available for female pups to reach sexual maturity. This suggests that not only does sex-ratio vary seasonally and among years, depending on the condition of the mother and the environment, but also likely varies geographically due to differences in season length.     

Parallel evolution of IDH2 gene in cetaceans,primates and bats

Cetaceans and primates both have large brains that require large amounts of aerobic energy metabolism. In bats, the cost of flight makes locomotion energetically demanding. These mammalian groups may represent three independent evolutionary origins of an energy-demanding lifestyle in mammals. IDH2 encodes an enzyme in the tricarboxylic acid cycle in the mitochondrion, which plays a key role in aerobic energy metabolism. In this study, we cloned and sequenced this gene in two cetaceans, and 19 bat species, and compared the data with available primate sequences to test its evolution. We found significant signals of parallel evolution in this gene among these three groups. Parallel evolution of this gene may reflect their parallel evolution towards a higher demand for energy.     

Optimization of reproductive effort and foraging time in mammals: The influence of resource level and predation risk

Summary The trade-off between fitness benefits from foraging and associated costs in terms of predation risk is analysed by a simple model which takes into account the differential predation risk for reproducing and non-reproducing individuals. The currency that animals are assumed to maximize is their expected absolute fitness (probability of survival plus half of the expected litter size) after a potential reproductive period. Depending on resource levels and predation risk, this maximization can be achieved by (1) opting for individual survival and behaving as a strict time minimizer, (2) by reproducing at the maximal rate and behaving as a strict energy maximizer or (3) by submaximal reproductive effort and a behaviour intermediate between time minimization and energy maximization. Small changes in the availability of food or cover or in the density of predators can shift the optimum from one strategy to another. The shift is particularly abrupt, if predation pressure increases and the availability of resources remains high. This could explain the spatial and temporal variation in the reproductive effort and body weight observed in boreal small mammals with sustained, multiannual population fluctuations.     

Costs of reproduction in a population of European adders

Eleven years of data on a small population of adders (Vipera berus) in southern Sweden provide quantitative information on the nature and degree of costs faced by reproducing animals. Reproduction imposes both an energy cost (measured by loss in body mass) and a mortality cost on adders of both sexes. The extent of the energy cost is broadly independent of levels of reproductive activity in males, but mortality costs are highest for large males, perhaps because they are more obvious to predators. In females, energy costs include a high ‘fixed’ (fecundity-independent) component, such that a large litter may cost little more to produce than would a small litter. Energy costs and mortality costs are separate in males, but inter-related in females. Mortality of reproducing females is high (40% per year), primarily because post-parturient females are emaciated and must forage actively, hence increasing their vulnerability to predators. Females producing relatively large litters (high Relative Clutch Mass) lose more body mass, and are less likely to survive after reproducing. The observed low reproductive frequencies of female adders may result from the presence of high fecundity-independent costs of reproduction.     

Metabolic compensation during high energy output in fasting, lactating grey seals (Halichoerus grypus): metabolic ceilings revisited

Lactation is the most energetically expensive period for female mammals and is associated with some of the highest sustained metabolic rates (SusMR) in vertebrates (reported as total energy throughput). Females typically deal with this energy demand by increasing food intake and the structure of the alimentary tract may act as the central constraint to ceilings on SusMR at about seven times resting or standard metabolic rate (SMR). However, demands of lactation may also be met by using a form of metabolic compensation such as reducing locomotor activities or entering torpor. In some phocid seals, cetaceans and bears, females fast throughout lactation and thus cannot offset the high energetic costs of lactation through increased food intake. We demonstrate that fasting grey seal females sustain, for several weeks, one of the highest total daily energy expenditures (DEE; 7.4 x SMR) reported in mammals, while progressively reducing maintenance metabolic expenditures during lactation through means not explained by reduction in lean body mass or behavioural changes. Simultaneously, the energy-exported in milk is progressively increased, associated with increased lipoprotein lipase activity in the mammary gland, resulting in greater offspring growth. Our results suggest that females use compensatory mechanisms to help meet the extraordinary energetic costs of lactation. Additionally, although the concepts of SusMR and ceilings on total DEE may be somewhat different in fasting lactating species, our data on phocid seals demonstrate that metabolic ceilings on milk energy output, in general, are not constrained by the same kind of peripheral limitations as are other energy-consuming tissues. In phocid seals, the high ceilings on DEE during lactation, coupled with metabolic compensation, are undoubtedly important factors enabling shortened lactation.     

Diapause affects cuticular hydrocarbon composition and mating behavior of both sexes in Drosophila montana

Envipnmental cues,mainly photoperiod and temperature,are known to control female adult reproductive diapause in several insect species.Diapause enhances female survival during adverse conditions and postpones progeny production to the favorable season.Male diapause(a reversible inability to inseminate receptive females)has been studied much less than female diapause.However,if the males maximized their chances to fertilize females while minimizing their energy expenditure,they would be expected to be in diapause at the same time as females.We investigated Drosophila montana male mating bchavior under short-day conditions that induce diapause in females and found the males to be reproductively inactive.We also found that males reared under long-day conditions(reproducing individuals)court reproducing postdiapause fermales,but not diapausing ones.The diapausing fies of both sexes had more long-chain and less short-chain hydrocarbons on their cuticle than the reproducing ones,which presumably increase their survival under stressful conditions,but at the same time decrease their attractiveness.Our study shows that the mating behavior of females and males is well coordinated during and afier overwintering and it also gives support to the dual role of insect cuticular hydrocarbons in adaptation and mate choice.     

The influence of androgenic steroid hormones on female aggression in ‘atypical’ mammals

Dimorphism on dominance and agonistic behaviour in mammals tends to be strongly biased toward males. In this review, we focus on a select few species of mammals in which females are as or more aggressive than males, and/or are dominant to males, and explore the role of androgenic hormones in mediating this important difference. While the data are not as clear-cut as those published on traditional laboratory mammals, our review highlights important endocrine substrates for both organizational and activational influences of steroids on female aggressive behaviour. We highlight areas in which further observations and experiments are crucial, especially the potential facilitative effects of androgens on female aggression. Finally, new and innovative techniques, including molecular genetics and receptor pharmacology, portend important insights into the ways in which androgenic hormones regulate aggressive behaviour in ‘atypical’ female mammals.     

Synthetic fragments of the CD4 receptor cytoplasmic domain and large polycations alter the activities of the pp56lck tyrosine protein kinase

In CD4+ T cells, the src-like tyrosine kinase pp56lck is associated with the CD4 receptor and cross-linking of CD4 results in the activation of this enzyme. The mechanism responsible for this activation is not known, although there is evidence that the activities of the src family of enzymes are regulated by tyrosine phosphorylation. Here we report that pp56lck-catalyzed angiotensin II phosphorylations are activated 20-fold in vitro by synthetic peptides reproducing portions of the murine CD4 cytoplasmic domain. This activation is described by a dissociation constant of about 2 microM. The pp56lck-catalyzed phosphorylation of other peptide substrates are effected less and in one case not at all by the peptide modulators, indicating that these CD4 sequences alter the substrate specificity of pp56lck. In contrast, peptides reproducing sequences from the CD8 receptor have a charge and size similar to the CD4 peptides, yet are vastly less effective at modulating pp56lck activities. High ionic strengths inhibit the CD4 peptide-induced modulation of pp56lck phosphotransferase activities, suggesting that charge-charge interactions are important for this process. In addition, the modulation of pp56lck activities by peptides reproducing the CD4 cytoplasmic domain are reproduced by polycations significantly larger than the CD4 cytoplasmic domain but not by those of similar size. The modulations both by CD4 peptides and the polycations do not depend on enzyme tyrosine phosphorylations.     

Does osteoderm growth follow energy minimization principles?

Although the growth and development of tissues and organs of extinct species cannot be directly observed, their fossils can record and preserve evidence of these mechanisms. It is generally accepted that bone architecture is the result of genetically based biomechanical constraints, but what about osteoderms? In this article, the influence of physical constraints on cranial osteoderms growth is assessed. Comparisons among lepidosaurs, synapsids, and archosaurs are performed; according to these analyses, lepidosaur osteoderms growth is predicted to be less energy demanding than that of synapsids and archosaurs. Obtained results also show that, from an energetic viewpoint, ankylosaurid osteoderms growth resembles more that of mammals than the one of reptilians, adding evidence to debate whether dinosaurs were hot or cold blooded. J. Morphol. 275:923–932, 2014. © 2014 Wiley Periodicals, Inc.     

Mild mitochondrial uncoupling in mice affects energy metabolism, redox balance and longevity

Caloric restriction is the most effective non-genetic intervention to enhance lifespan known to date. A major research interest has been the development of therapeutic strategies capable of promoting the beneficial results of this dietary regimen. In this sense, we propose that compounds that decrease the efficiency of energy conversion, such as mitochondrial uncouplers, can be caloric restriction mimetics. Treatment of mice with low doses of the protonophore 2,4-dinitrophenol promotes enhanced tissue respiratory rates, improved serological glucose, triglyceride and insulin levels, decrease of reactive oxygen species levels and tissue DNA and protein oxidation, as well as reduced body weight. Importantly, 2,4-dinitrophenol-treated animals also presented enhanced longevity. Our results demonstrate that mild mitochondrial uncoupling is a highly effective in vivo antioxidant strategy, and describe the first therapeutic intervention capable of effectively reproducing the physiological, metabolic and lifespan effects of caloric restriction in healthy mammals.     

Physiological Costs of Repetitive Courtship Displays in Cockroaches Handicap Locomotor Performance

Courtship displays are typically thought to have evolved via female choice, whereby females select mates based on the characteristics of a display that is expected to honestly reflect some aspect of the male’s quality. Honesty is typically enforced by mechanistic costs and constraints that limit the level at which a display can be performed. It is becoming increasingly apparent that these costs may be energetic costs involved in the production of dynamic, often repetitive displays. A female attending to such a display may thus be assessing the physical fitness of a male as an index of his quality. Such assessment would provide information on his current physical quality as well as his ability to carry out other demanding activities, qualities with which a choosy female should want to provision her offspring. In the current study we use courtship interactions in the Cuban burrowing cockroach, Byrsotria fumigata to directly test whether courtship is associated with a signaler’s performance capacity. Males that had produced courtship displays achieved significantly lower speeds and distances in locomotor trials than non-courting control males. We also found that females mated more readily with males that produced a more vigorous display. Thus, males of this species have developed a strategy where they produce a demanding courtship display, while females choose males based on their ability to produce this display. Courtship displays in many taxa often involve dynamic repetitive actions and as such, signals of stamina in courtship may be more widespread than previously thought.     

Increased parasite abundance associated with reproductive maturity of the clam Anodonta piscinalis.

Several studies on vertebrates have demonstrated that reproductive activities may increase the parasite load, but this has not been shown in invertebrate hosts. We studied abundance of a potentially harmful gill parasite, the ergasilid copepod Paraergasilus rylovi, from the freshwater bivalve host Anodonta piscinalis in relation to reproductive maturity of the host in the field. Prevalence of this previously unstudied parasite varied from 90 to 100%, and the mean parasite abundance from 16.3 to 28.8 among 3 study populations. Abundance of P. rylovi increased with host size. In the maturating age groups (3-5 yr) the length-adjusted mean parasite abundance among mature, reproducing female clams that brooded glochidia larvae was 2 times higher than in nonreproducing females, the observed pattern being consistent among the 3 study lakes. Alternative, mutually nonexclusive explanations may be found for the result. For example, changes in clam behavior or filtration activity accompanying maturation can increase host exposure to parasites, or reproduction may decrease energy available to host immunologic defense. However, the present result indicates that maturation, and reproduction, is associated with increased parasite abundance in A. piscinalis, an invertebrate host.     

The energetic cost of mating in a promiscuous cephalopod

Costs that individuals incur through mating can play an important role in understanding the evolution of life histories and senescence, particularly in promiscuous species. Copulation costs, ranging from energy expenditure to reduced longevity, are widely studied in insects but have received substantially less attention in other taxa. One cost of mating, the energetic cost, is poorly studied across all taxa despite its potential importance for the many species where copulation is physically demanding and/or frequent. Here, we investigated the energetic cost of mating in both male and female dumpling squid (Euprymna tasmanica). In this species, copulation can last up to 3 h and requires that the male physically restrains the female. We report that the act of copulation halves the swimming endurance of both sexes, and that they take up to 30 min to recover. Such a reduction in post-copulatory performance may have important implications for predator avoidance, foraging ability and energy allocation. Therefore, quantifying this cost is essential to understand the evolution of reproductive strategies and behaviours such as female receptivity and male and female mating frequency.     

Loss of function of MULTICOPY SUPPRESSOR OF IRA 1 produces nonviable parthenogenetic embryos in Arabidopsis

In sexually reproducing species, fertilization brings together in the zygote the genomes of the female and male gametes. In several animal species, female gametes are able to initiate embryogenesis in the absence of fertilization, a process referred to as parthenogenesis. Parthenogenesis has been engineered in mice by tampering with expression of loci under epigenetic controls [1]. In plants, embryo development in the absence of fertilization has been reported in cases in which meiosis is bypassed leading to apomictic development, and parthenogenetic development from a reduced egg cell has been only reported in rare accidental cases [2]. We report that single mutations in the gene MULTICOPY SUPPRESSOR OF IRA 1 (MSI1) are able to initiate parthenogenetic development of the embryo in Arabidopsis thaliana from eggs cells produced by meiosis. The WD40 repeat protein MSI1 is part of the evolutionarily conserved Polycomb group (PcG) chromatin-remodeling complexes [3] and is homologous to the Retinoblastoma binding proteins P55 in Drosophila and RbAp48 in mammals [4]. Nonviable haploid parthenogenetic msi1 embryos express molecular markers and polarity similar to diploid wild-type (wt) embryos produced by fertilization, indicating a maternal contribution to early patterning of the Arabidopsis embryo.     

Why are (the best) women so good at chess? Participation rates and gender differences in intellectual domains

A popular explanation for the small number of women at the top level of intellectually demanding activities from chess to science appeals to biological differences in the intellectual abilities of men and women. An alternative explanation is that the extreme values in a large sample are likely to be greater than those in a small one. Although the performance of the 100 best German male chess players is better than that of the 100 best German women, we show that 96 per cent of the observed difference would be expected given the much greater number of men who play chess. There is little left for biological or cultural explanations to account for. In science, where there are many more male than female participants, this statistical sampling explanation, rather than differences in intellectual ability, may also be the main reason why women are under-represented at the top end.     

Daily Energy Expenditure and the Cost of Activity in Mammals

Among 17 species of mammals, field metabolic rates exclusiveof thermoregulatory and productive costs (designated FMR*) averaged2.65 x standard metabolism (SMR). Daily activity costswere calculatedby subtraction from FMR* of the daily energy expenditure associatedwith SMR and assimilation of nutrients. Total expenditure foractivity was of a similar magnitude to that for daily standardmetabolism. Calculations indicate that expenditures by mammalsfor locomotion probably account for less than half of dailyactivity costs. Expenditures by mammals engaged in other kindsof activities are also reviewed. During their daily activityperiods, terrestrial mammals expend energy at a rate of about4.1 x SMR. The utility of energetic increments for activityin time-energy budgets, thermal energy budgets, and analysesof the economics of foraging are discussed.