Meta-analysis reveals that resting metabolic rate is not consistently related to fitness and performance in animals

Explaining variation in the fitness of organisms is a fundamental goal in evolutionary ecology. Maintenance energy metabolism is the minimum energy required to sustain biological processes at rest (resting metabolic rate: RMR) and is proposed to drive or constrain fitness of animals; however, this remains debated. Hypotheses have been proposed as to why fitness might increase with RMR (the 'increased intake' or 'performance' hypothesis), decrease with RMR (the 'compensation' or 'allocation' hypothesis), or vary among species and environmental contexts (the 'context dependent' hypothesis). Here, we conduct a systematic review and meta-analysis of the literature, finding 114 studies with 355 relationships between RMR and traits that may be related to fitness. We show that individuals with relatively high RMR generally have high fitness overall, which might be supported by an increased energy intake. However, fitness proxies are not interchangeable: the nature of the RMR-fitness relationship varied substantially depending on the specific trait in question, and we found no consistent relationship between RMR and those traits most closely linked with actual fitness (i.e., lifetime reproductive success). We hypothesise that maintaining high RMR is not costly when resources are unlimited, and we propose ideas for future studies to identify mechanisms underlying RMR-fitness relationships.This research was supported by grants from the Australian Research Council

Spatial and temporal variation in the effects of climatic variables on Dugong calf production

Knowledge of the relationships between environmental forcing and demographic parameters is important for predicting responses from climatic changes and to manage populations effectively. We explore the relationships between the proportion of sea cows (Dugong dugon) classified as calves and four climatic drivers (rainfall anomaly, Southern Oscillation El Niño Index [SOI], NINO 3.4 sea surface temperature index, and number of tropical cyclones) at a range of spatially distinct locations in Queensland, Australia, a region with relatively high dugong density. Dugong and calf data were obtained from standardized aerial surveys conducted along the study region. A range of lagged versions of each of the focal climatic drivers (1 to 4 years) were included in a global model containing the proportion of calves in each population crossed with each of the lagged versions of the climatic drivers to explore relationships. The relative influence of each predictor was estimated via Gibbs variable selection. The relationships between the proportion of dependent calves and the climatic drivers varied spatially and temporally, with climatic drivers influencing calf counts at sub-regional scales. Thus we recommend that the assessment of and management response to indirect climatic threats on dugongs should also occur at sub-regional scales. © 2016 Fuentes et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

Development and evaluation of a custom bait design based on 469 single-copy protein-coding genes for exon capture of isopods (Philosciidae: Haloniscus)

Transcriptome-based exon capture approaches, along with next-generation sequencing, are allowing for the rapid and cost-effective production of extensive and informative phylogenomic datasets from non-model organisms for phylogenetics and population genetics research. These approaches generally employ a reference genome to infer the intron-exon structure of targeted loci and preferentially select longer exons. However, in the absence of an existing and well-annotated genome, we applied this exon capture method directly, without initially identifying intron-exon boundaries for bait design, to a group of highly diverse Haloniscus (Philosciidae), paraplatyarthrid and armadillid isopods, and examined the performance of our methods and bait design for phylogenetic inference. Here, we identified an isopod-specific set of single-copy protein-coding loci, and a custom bait design to capture targeted regions from 469 genes, and analysed the resulting sequence data with a mapping approach and newly-created post-processing scripts. We effectively recovered a large and informative dataset comprising both short (300 bp) exons, with high uniformity in sequencing depth. We were also able to successfully capture exon data from up to 16-year-old museum specimens along with more distantly related outgroup taxa, and efficiently pool multiple samples prior to capture. Our well-resolved phylogenies highlight the overall utility of this methodological approach and custom bait design, which offer enormous potential for application to future isopod, as well as broader crustacean, molecular studies

Predictors of contraction and expansion of area of occupancy for British birds

Copyright © 2014 The Author(s) Published by the Royal SocietyGeographical range dynamics are driven by the joint effects of abiotic factors, human ecosystem modifications, biotic interactions and the intrinsic organismal responses to these. However, the relative contribution of each component remains largely unknown. Here, we compare the contribution of life-history attributes, broad-scale gradients in climate and geographical context of species’ historical ranges, as predictors of recent changes in area of occupancy for 116 terrestrial British breeding birds (74 contractors, 42 expanders) between the early 1970s and late 1990s. Regional threat classifications demonstrated that the species of highest conservation concern showed both the largest contractions and the smallest expansions. Species responded differently to climate depending on geographical distribution—northern species changed their area of occupancy (expansion or contraction) more in warmer and drier regions, whereas southern species changed more in colder and wetter environments. Species with slow life history (larger body size) tended to have a lower probability of changing their area of occupancy than species with faster life history, whereas species with greater natal dispersal capacity resisted contraction and, counterintuitively, expansion. Higher geographical fragmentation of species' range also increased expansion probability, possibly indicating a release from a previously limiting condition, for example through agricultural abandonment since the 1970s. After accounting statistically for the complexity and nonlinearity of the data, our results demonstrate two key aspects of changing area of occupancy for British birds: (i) climate is the dominant driver of change, but direction of effect depends on geographical context, and (ii) all of our predictors generally had a similar effect regardless of the direction of the change (contraction versus expansion). Although we caution applying results from Britain's highly modified and well-studied bird community to other biogeographic regions, our results do indicate that a species' propensity to change area of occupancy over decadal scales can be explained partially by a combination of simple allometric predictors of life-history pace, average climate conditions and geographical context.Australian Research CouncilIntegrated Program of IC&DTFCT (Fundação para a Ciência e a Tecnologia

Longitudinal population demography of the allied rock-wallaby, Petrogale assimilis

The allied rock-wallaby, Petrogale assimilis, is a medium-sized, monomorphic,\ud continuously-breeding macropodid marsupial that lives in rocky habitats in the climatically\ud unpredictable wet-dry tropics of north-eastern Australia. Long-term capture-recapture records of individually marked P. assimilis from an isolated population inhabiting Black Rock, a sandstone escarpment in western Queensland, were used to investigate the population demography of the species over 12 years.\ud \ud In natural populations, both extrinsic environmental variation and intrinsic density-dependence\ud contribute to variability in demographic fitness components. Changes in these fitness\ud components, and trade-offs between them, determine the dynamics of populations. Almost no\ud information is available on the temporal variability of the demographic fitness components and\ud their relationship with rates of population change for kangaroos and wallabies. This research\ud provides the first long-term study of a macropod species that is based on individually-marked\ud animals, which are required to estimate such fitness components and their temporal variation. A major aim of this research was to determine the impact of variability in the fitness components on the population dynamics of this macropod species, and to compare these results with those available for other long-lived herbivores. The demographic components of the life history of P. assimilis at Black Rock were investigated, along with the interrelationships between long-term temporal variability in these components and intrinsic and extrinsic factors, and individual fitness. The long-term fitness of the population and the influence of temporal covariation between the demographic components on variability in population fitness were also examined.\ud \ud The growth relationship between the size and age of P. assimilis at Black Rock was determined using various nonlinear models within a mixed-effects framework. The age and individual variation in growth of animals of unknown age were estimated from measurements of body size. Parametric nonlinear models did not fit the growth pattern, but semi-parametric spline models adequately described the growth pattern and accounted for individual variation. Differences in growth between the sexes were small, suggesting no strong sexual size dimorphism in P. assimilis. Growth rates were highest during pouch development, were lower during the weaning period, and decreased dramatically after weaning. The age structure of the population of P. assimilis at Black Rock varied substantially over the study period.\ud \ud The log-transformed relationships between body mass and various body size measures were\ud nonlinear and the head length was the best predictor of body mass of P. assimilis at Black\ud Rock. Indices of body condition were calculated from the residuals of mixed-effects models that estimated the form of the size-mass relationship using splines. Substantial variation in body condition was explained by annual and seasonal variability and lagged rainfall, as well as variation between individual animals. Variation in body condition was not associated with sex or age-class, and did not depend on the lactation status of females. The estimated index of body condition appeared to represent the nutritional status of individual P. assimilis at Black Rock and was used as a predictor of variation in demographic rates associated with individual fitness.\ud \ud Directional goodness-of-fit tests for Cormack-Jolly-Seber capture-recapture models showed\ud that individual P. assimilis at Black Rock had a trap happy response to capture. The likelihood\ud of recapture varied over time and depended on whether animals were captured on the previous sampling occasion. Recapture probability was generally very high, and was lower for adult females not marked as young than for other females marked as young and for all males,\ud regardless of age at marking. Similar effects on recapture probability were identified using\ud generalised linear mixed models, though the time-dependent effect could be simplified to a year by season interaction plus the effect of trapping effort. There was strong agreement between estimates of population size based on different methods. Population size fluctuated\ud substantially over the study with periods of consistent increase and decline, and showed\ud evidence of rapid population recovery from relatively low numbers under positive environmental conditions.\ud \ud Support for the Trivers-Willard hypothesis (TWH), which states that if the costs of reproduction differ between the sexes then the offspring sex ratio will vary depending on the parent’s ability to allocate resources, was evaluated. The sex ratio at birth was equal and not correlated with mother’s age, body mass or body condition. Sex ratio varied seasonally; being female-biased in the mid- to late-dry season and male-biased in the late dry and early wet seasons. Survival from birth to pouch emergence was correlated with environmental conditions, depending on sex, in the direction consistent with TWH; male survival was higher than female survival under good conditions and lower under poor conditions. Also, survival was higher for pouch young of heavier mothers or mothers in good condition. Survival to pouch emergence was also density-dependent. In support of TWH, the sex ratio at pouch emergence was male-biased under good environmental conditions and was male-biased for mothers in good condition or heavier mothers. Mothers in good condition produced offspring in good condition, satisfying an assumption of TWH, and higher mass at pouch emergence resulted in improved survivorship to weaning.\ud \ud Survival from pouch emergence to weaning was higher for females than males, and was\ud positively correlated with environmental conditions. Females had higher survival to weaning\ud than males in the hotter seasons, but there was no sex difference in survival in the cooler\ud seasons. Survival was also higher for females than for males born to lighter mothers, but there\ud was no difference between the sexes born to heavier mothers. Male-biased sex ratios at\ud weaning were observed under good environmental conditions and for mothers with higher body\ud mass, providing support for TWH at this life history stage. The body mass of offspring at weaning was correlated with maternal body mass, satisfying an assumption of TWH, and\ud offspring mass was also higher under high rainfall conditions. Patterns of variability in the sex\ud ratio and pre-weaning survival of P. assimilis at Black Rock were influenced by a combination\ud of: (1) adaptive allocation of resources between the sexes depending on maternal condition;\ud and (2) non-adaptive extrinsic modification associated with environmental stochasticity, allowing\ud mothers to respond quickly in a variable environment to maximise their current reproduction and\ud future survival.\ud \ud Male P. assimilis matured later and were heavier at maturity than females. Early maturity was\ud favoured for females but not for males under high rainfall conditions, independent of size at\ud maturity. Age at maturity was density-dependent for males only, with delayed maturity at lower\ud population sizes. Maturation was delayed for both sexes when body mass at weaning was low\ud relative to individuals with high weaning mass.\ud \ud Subadult male survival was lower than for females, and survival of both sexes increased under\ud high rainfall conditions. Adult survival was higher than subadult survival, independent of sex,\ud and survival of older adults was lower than that of prime-aged adults, indicating senescence.\ud Survival increased under positive climatic conditions and was density-dependent, with lower\ud survival at high population sizes. Males had lower survival to sexual maturity than females, and\ud increased body mass improved survival for both sexes. Population growth rate was most\ud sensitive to changes in prime-aged adult survival, as is typical for longer-lived vertebrates. The\ud temporal variance in the juvenile survival stages was much higher than in adult survival.\ud Therefore, consistent with other longer-lived, iteroparous vertebrates, the impact of relative\ud changes to adult survival on population growth were much greater than changes of the same\ud magnitude to either survival in the juvenile stages, or to the fecundity rate.\ud \ud There was a negative relationship between temporal variation in the demographic rates and\ud their sensitivities, indicating that the more variable vital rates had low effects on long-term\ud population growth. The most variable demographic rates covaried suggesting that common\ud factors contributed to temporal variability. Covariation in survival between the juvenile and\ud pre-maturity life history stages accounted for most of the variability in the population growth\ud rate, indicating survivorship in the juvenile stages was more important than adult survival in\ud determining changes in the population growth rate of P. assimilis at Black Rock. The survival\ud patterns of different life history stages were variable for P. assimilis at Black Rock, and\ud responded differently to environmental variability and population density. Density-dependent\ud and density-independent limiting factors primarily acted on the juvenile survival components of\ud the life history, and covariation among these fitness components influenced the dynamics of the\ud population. Survival of prime-aged adult P. assimilis at Black Rock was much less sensitive to \ud these limiting factors, showed the highest elasticity, and appeared to be buffered against\ud temporal variability. These results add to growing evidence from natural populations that natural\ud selection may favour traits that are highly buffered against environmental variability.\u

Reproduction of the purple-necked rock-wallaby, Petrogale purpureicollis Le Souef (Marsupialia : Macropodidae) in captivity, with age estimation and development of the pouch young

Reproduction of the purple-necked rock-wallaby, Petrogale purpureicollis, was studied in captivity. The length of the oestrous cycle was 36–38 days followed by a gestation period of 33–35 days. Birth was usually followed by an oestrus and mating, and a subsequent lactation-controlled embryonic diapause. The interval between loss of pouch young and birth was 30–36 days. Pouch life was 178–197 days and weaning occurred 92–171 days after permanent emergence from the pouch. The youngest age at which sexual maturity was reached was 21.8 months for males and 18 months for females. Linear mixed-effects models were used to describe polynomial growth equations for age determination of pouch young using both head and pes length. The relationship between error in age prediction and each body measurement was also defined. Head measurements provided the most accurate estimates of the age of pouch young

Reproduction in the northern bettong, Bettongia tropica Wakefield (Marsupialia: Potoroidae), in captivity, with age estimation and development of pouch young

Reproduction in the northern bettong, Bettongia tropica, was studied in captivity. B. tropica is capable of breeding throughout the year, and mating behaviour is similar to that reported for other Bettongia species. The length of the oestrous cycle was 21–23 days, and the period of gestation was 20–23 days. Birth was usually followed by an oestrus and mating, and a subsequent lactation-controlled embryonic diapause. The interval between loss of pouch young and birth was 19–20 days. Permanent emergence from the pouch occurred at 102–112 days, and young at foot were weaned at 166–185 days of age. Linear mixed-effects models were used to describe polynomial growth equations for age determination of pouch young using both head and pes length. The relationship between error in age prediction and each body measurement was also defined. Pes measurements provided the most accurate estimates of the age of pouch young

Climate and maternal effects modify sex ratios in a weakly dimorphic marsupial

Abstract There is growing evidence that the sex ratios of wild vertebrate populations are determined by mechanisms that are directly influenced by environmental characteristics. The Trivers-Willard (TWH) and extrinsic modification (EMH) hypotheses postulate differing determinants of mammalian offspring sex ratios. TWH states that mothers allocate resources according to their current condition and sex-specific offspring costs. EMH states that environmental forces that affect maternal condition determine offspring sex ratios, independently of maternal tactics of sex-biased allocation. We statistically assessed support for each of these hypotheses using long-term life histories of the allied rock-wallaby, Petrogale assimilis; a continuously breeding, polygynous, weakly dimorphic marsupial. We showed that birth sex ratios were equal and independent of maternal and environmental conditions. However, secondary sex ratios were male-biased under good environmental conditions and for high quality mothers or mothers in good condition. Sex differences in offspring survival contributed to these biases: (1) environmental conditions strongly influenced survival to pouch emergence (in support of EMH) and (2) maternal quality affected survival to the end of maternal care (in support of TWH). Environmental effects on survival were more important than maternal factors over the entire period of maternal care and contributed most to male-biased sex ratios at pouch emergence. In contrast, maternal mass was the best predictor of sex ratios at the end of maternal carethe life history stage where offspring body mass differed between the sexes

Phylogeny and the selectivity of extinction in Australian marsupials

Recent studies have suggested that contemporary losses of species are unevenly distributed over phylogenies. Here, we show that species of Australian marsupials are at higher risk if they belong to genera that are species-poor, old or phylogenetically distinct. Extinction risk in this group is also related to habitat and body size, being higher for species from non-forested habitats and of intermediate body size. We tested the extent to which the phylogenetic selectivity of extinction was explained by this ecological pattern. We found that while genus size and distinctiveness explain no variation in extinction risk that is not accounted for by habitat and body size, there is a significant residual association of genus age with extinction risk. This suggests that while species in small and distinctive genera are at high risk because they are overrepresented in non-forested habitats and intermediate body size classes, species in old genera are at higher risk over the range of body sizes and habitats and may be intrinsically vulnerable to extinction