Sleep in the wild: the importance of individual effects and environmental conditions on sleep behaviour in wild boar.

Sleep serves vital physiological functions, yet how sleep in wild animals is influenced by environmental conditions is poorly understood. Here we use high-resolution biologgers to investigate sleep in wild animals over ecologically relevant time scales and quantify variability between individuals under changing conditions. We developed a robust classification for accelerometer data and measured multiple dimensions of sleep in the wild boar (Sus scrofa) over an annual cycle. In support of the hypothesis that environmental conditions determine thermoregulatory challenges, which regulate sleep, we show that sleep quantity, efficiency and quality are reduced on warmer days, sleep is less fragmented in longer and more humid days, while greater snow cover and rainfall promote sleep quality. Importantly, this longest and most detailed analysis of sleep in wild animals to date reveals large inter- and intra-individual variation. Specifically, short-sleepers sleep up to 46% less than long-sleepers but do not compensate for their short sleep through greater plasticity or quality, suggesting they may pay higher costs of sleep deprivation. Given the major role of sleep in health, our results suggest that global warming and the associated increase in extreme climatic events are likely to negatively impact sleep, and consequently health, in wildlife, particularly in nocturnal animals.

Human activities favour prolific life histories in both traded and introduced vertebrates.

Species' life histories determine population demographics and thus the probability that introduced populations establish and spread. Life histories also influence which species are most likely to be introduced, but how such 'introduction biases' arise remains unclear. Here, we investigate how life histories affect the probability of trade and introduction in phylogenetic comparative analyses across three vertebrate classes: mammals, reptiles and amphibians. We find that traded species have relatively high reproductive rates and long reproductive lifespans. Within traded species, introduced species have a more extreme version of this same life history profile. Species in the pet trade also have long reproductive lifespans but lack 'fast' traits, likely reflecting demand for rare species which tend to have slow life histories. We identify multiple species not yet traded or introduced but with life histories indicative of high risk of future trade, introduction and potentially invasion. Our findings suggest that species with high invasion potential are favoured in the wildlife trade and therefore that trade regulation is crucial for preventing future invasions.

The reproductive ecology drivers of egg attendance in amphibians.

Parental care is extremely diverse but, despite much research, why parental care evolves is poorly understood. Here we address this outstanding question using egg attendance, the simplest and most common care form in many taxa. We demonstrate that, in amphibians, terrestrial egg deposition, laying eggs in hidden locations and direct development promote the evolution of female egg attendance. Male egg attendance follows the evolution of hidden eggs and is associated with terrestrial egg deposition but not with direct development. We conclude that egg attendance, particularly by females, evolves following changes in reproductive ecology that are likely to increase egg survival, select for small clutches of large eggs and/or expose eggs to new environmental challenges. While our results resolve a long-standing question on whether reproductive ecology traits are drivers, consequences or alternative solutions to caring, they also unravel important, yet previously unappreciated, differences between the sexes.

Switches, stability and reversals in the evolutionary history of sexual systems in fish.

Sexual systems are highly diverse and have profound consequences for population dynamics and resilience. Yet, little is known about how they evolved. Using phylogenetic Bayesian modelling and a sample of 4614 species, we show that gonochorism is the likely ancestral condition in teleost fish. While all hermaphroditic forms revert quickly to gonochorism, protogyny and simultaneous hermaphroditism are evolutionarily more stable than protandry. In line with theoretical expectations, simultaneous hermaphroditism does not evolve directly from gonochorism but can evolve slowly from sequential hermaphroditism, particularly protandry. We find support for the predictions from life history theory that protogynous, but not protandrous, species live longer than gonochoristic species and invest the least in male gonad mass. The distribution of teleosts' sexual systems on the tree of life does not seem to reflect just adaptive predictions, suggesting that adaptations alone may not fully explain why some sexual forms evolve in some taxa but not others (Williams' paradox). We propose that future studies should incorporate mating systems, spawning behaviours, and the diversity of sex determining mechanisms. Some of the latter might constrain the evolution of hermaphroditism, while the non-duality of the embryological origin of teleost gonads might explain why protogyny predominates over protandry in teleosts.

Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians.

The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.

A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae).

The Sparids are an ideal group of fishes in which to study the evolution of sexual systems since they exhibit a great sexual diversity, from gonochorism (separate sexes) to protandrous (male-first) and protogynous (female-first) sequential hermaphroditism (sex change). According to the size-advantage model (SAM), selection should favour sex change when the second sex achieves greater reproductive success at a larger body size than the first sex. Using phylogenetic comparative methods and a sample of 68 sparid species, we show that protogyny and protandry evolve from gonochorism but evolutionary transitions between these two forms of sequential hermaphroditism are unlikely to happen. Using male gonadosomatic index (GSI) as a measure of investment in gametes and proxy for sperm competition, we find that, while gonochoristic and protogynous species support the predictions of SAM, protandrous species do not, as they exhibit higher GSI values than expected even after considering mating systems and spawning modes. We suggest that small males of protandrous species have to invest disproportionally more in sperm production than predicted not only when spawning in aggregations, with high levels of sperm competition, but also when spawning in pairs due to the need to fertilize highly fecund females, much larger than themselves. We propose that this compensatory mechanism, together with Bateman's principles in sequential hermaphrodites, should be formally incorporated in the SAM.

The evolution of parental care diversity in amphibians.

Parental care is extremely diverse across species, ranging from simple behaviours to complex adaptations, varying in duration and in which sex cares. Surprisingly, we know little about how such diversity has evolved. Here, using phylogenetic comparative methods and data for over 1300 amphibian species, we show that egg attendance, arguably one of the simplest care behaviours, is gained and lost faster than any other care form, while complex adaptations, like brooding and viviparity, are lost at very low rates, if at all. Prolonged care from the egg to later developmental stages evolves from temporally limited care, but it is as easily lost as it is gained. Finally, biparental care is evolutionarily unstable regardless of whether the parents perform complementary or similar care duties. By considering the full spectrum of parental care adaptations, our study reveals a more complex and nuanced picture of how care evolves, is maintained, or is lost.

Unravelling the macro-evolutionary ecology of fish-jellyfish associations: life in the 'gingerbread house'.

Fish-jellyfish interactions are important factors contributing to fish stock success. Jellyfish can compete with fish for food resources, or feed on fish eggs and larvae, which works to reduce survivorship and recruitment of fish species. However, jellyfish also provide habitat and space for developing larval and juvenile fish which use their hosts as means of protection from predators and feeding opportunities, helping to reduce fish mortality and increase recruitment. Yet, relatively little is known about the evolutionary dynamics and drivers of such associations which would allow for their more effective incorporation into ecosystem models. Here, we found that jellyfish association is a probable adaptive anti-predator strategy for juvenile fish, more likely to evolve in benthic (fish living on the sea floor), benthopelagic (fish living just above the bottom of the seafloor), and reef-associating species than those adapted to other marine habitats. We also found that jellyfish association likely preceded the evolution of a benthic, benthopelagic, and reef-associating lifestyle rather than its evolutionary consequence, as we originally hypothesized. Considering over two-thirds of the associating fish identified here are of economic importance, and the wide-scale occurrence and diversity of species involved, it is clear the formation of fish-jellyfish associations is an important but complex process in relation to the success of fish stocks globally.

Mixed phylogenetic signal in fish toxicity data across chemical classes.

Chemical use in society is growing rapidly and is one of the five major pressures on biodiversity worldwide. Since empirical toxicity studies of pollutants generally focus on a handful of model organisms, reliable approaches are needed to assess sensitivity to chemicals across the wide variety of species in the environment. Phylogenetic comparative methods (PCM) offer a promising approach for toxicity extrapolation incorporating known evolutionary relationships among species. If phylogenetic signal in toxicity data is high, i.e., closely related species are more similarly sensitive as compared to distantly related species, PCM could ultimately help predict species sensitivity when toxicity data are lacking. Here, we present the largest ever test of phylogenetic signal in toxicity data by combining phylogenetic data from fish with acute mortality data for 42 chemicals spanning 10 different chemical classes. Phylogenetic signal is high for some chemicals, particularly organophosphate pesticides, but not necessarily for many chemicals in other classes (e.g., metals, organochlorines). These results demonstrate that PCM may be useful for toxicity extrapolation in untested species for those chemicals with clear phylogenetic signal. This study provides a framework for using PCM to understand the patterns and causes of variation in species sensitivity to pollutants.

Fast life history traits promote invasion success in amphibians and reptiles.

Competing theoretical models make different predictions on which life history strategies facilitate growth of small populations. While 'fast' strategies allow for rapid increase in population size and limit vulnerability to stochastic events, 'slow' strategies and bet-hedging may reduce variance in vital rates in response to stochasticity. We test these predictions using biological invasions since founder alien populations start small, compiling the largest dataset yet of global herpetological introductions and life history traits. Using state-of-the-art phylogenetic comparative methods, we show that successful invaders have fast traits, such as large and frequent clutches, at both establishment and spread stages. These results, together with recent findings in mammals and plants, support 'fast advantage' models and the importance of high potential population growth rate. Conversely, successful alien birds are bet-hedgers. We propose that transient population dynamics and differences in longevity and behavioural flexibility can help reconcile apparently contrasting results across terrestrial vertebrate classes.

Male care and life history traits in mammals.

Male care has energetic and opportunity costs, and is more likely to evolve when males gain greater certainty of paternity or when future mating opportunities are scarce. However, little is known about the substantial benefits that males may provide to females and offspring. Using phylogenetic comparative methods and a sample of over 500 mammalian species, we show that mammals in which males carry the offspring have shorter lactation periods, which leads to more frequent breeding events. Provisioning the female is associated with larger litters and shorter lactation. Offspring of species with male care have similar weaning mass to those without despite being supported by a shorter lactation period, implying that they grow faster. We propose that males provide an energetic contribution during the most expensive time of female reproduction, lactation, and that different male care behaviours increase female fecundity, which in turn helps males offset the costs of caring.

The role of life history traits in mammalian invasion success.

Why some organisms become invasive when introduced into novel regions while others fail to even establish is a fundamental question in ecology. Barriers to success are expected to filter species at each stage along the invasion pathway. No study to date, however, has investigated how species traits associate with success from introduction to spread at a large spatial scale in any group. Using the largest data set of mammalian introductions at the global scale and recently developed phylogenetic comparative methods, we show that human-mediated introductions considerably bias which species have the opportunity to become invasive, as highly productive mammals with longer reproductive lifespans are far more likely to be introduced. Subsequently, greater reproductive output and higher introduction effort are associated with success at both the establishment and spread stages. High productivity thus supports population growth and invasion success, with barriers at each invasion stage filtering species with progressively greater fecundity.

Phylogenetic signal in amphibian sensitivity to copper sulfate relative to experimental temperature.

The release of large quantities of chemicals into the environment represents a major source of environmental disturbance. In recent years, the focus of ecotoxicology has shifted from describing the effects of chemical contaminants on individual species to developing more integrated approaches for predicting and evaluating long term effects of chemicals across species and ecosystems. Traditional ecotoxicology is typically based on data of sensitivity to a contaminant of a few surrogate species and often considers little variability in chemical sensitivity within and among taxonomic groups. This approach assumes that evolutionary history and phylogenetic relatedness among species have little or no impact on species' sensitivity to chemical compounds. Few studies have tested this assumption. Using phylogenetic comparative methods and published data for amphibians, we show that sensitivity to copper sulfate, a commonly used pesticide, exhibits a strong phylogenetic signal when controlling for experimental temperature. Our results indicate that evolutionary history needs to be accounted for to make accurate predictions of amphibian sensitivity to this contaminant under different temperature scenarios. Since physiological and metabolic traits showing high phylogenetic signal likely underlie variation in species sensitivity to chemical stressors, future studies should evaluate and predict species vulnerability to pollutants using evolutionarily informed approaches.

Microparasites and Placental Invasiveness in Eutherian Mammals.

Placental invasiveness-the number of maternal tissue layers separating fetal tissues from maternal blood-is variable across mammalian species. Although this diversity is likely to be functionally important, variation in placental invasiveness remains unexplained. Here we test the hypothesis that increased risk of transplacental transmission of pathogens from the mother to the fetus promotes the evolution of non-invasive placentation, the most likely derived condition in eutherian mammals. Specifically, we predict that non-invasive placentation is associated with increased microparasite species richness relative to more invasive placental types, based on the assumption that higher numbers of microparasites in a population reflects greater risk of transplacental transmission to fetuses. As predicted, higher bacteria species richness is associated with non-invasive placentation. Protozoa species richness, however, shows the opposite pattern. Because invasive placentae facilitate the transfer of maternal antibodies to the fetus, we propose that the ancestral condition of invasive placentation is retained under selection for protection of newborns from higher risk of postnatal protozoan infection. Hence, our findings suggest that a tradeoff exists between protection against bacterial infection prenatally and protozoan infection postnatally. Future studies are needed to investigate how maternal prevalence of infection and the relative pre- versus postnatal risk of fetal infection by different microparasite groups vary among mammalian hosts in relation to placental invasiveness.

Maternal investment, life histories, and the costs of brain growth in mammals.

Brain size variation in mammals correlates with life histories: larger-brained species have longer gestations, mature later, and have increased lifespans. These patterns have been explained in terms of developmental costs (larger brains take longer to grow) and cognitive benefits (large brains enhance survival and increase lifespan). In support of the developmental cost hypothesis, we show that evolutionary changes in pre- and postnatal brain growth correlate specifically with duration of the relevant phases of maternal investment (gestation and lactation, respectively). We also find support for the hypothesis that the rate of fetal brain growth is related to the energy turnover of the mother. In contrast, we find no support for hypotheses proposing that costs are accommodated through direct tradeoffs between brain and body growth, or between brain growth and litter size. When the duration of maternal investment is taken into account, adult brain size is uncorrelated with other life history traits such as lifespan. Hence, the general pattern of slower life histories in large-brained species appears to be a direct consequence of developmental costs.

Adaptive evolution of four microcephaly genes and the evolution of brain size in anthropoid primates.

The anatomical basis and adaptive function of the expansion in primate brain size have long been studied; however, we are only beginning to understand the genetic basis of these evolutionary changes. Genes linked to human primary microcephaly have received much attention as they have accelerated evolutionary rates along lineages leading to humans. However, these studies focus narrowly on apes, and the link between microcephaly gene evolution and brain evolution is disputed. We analyzed the molecular evolution of four genes associated with microcephaly (ASPM, CDK5RAP2, CENPJ, MCPH1) across 21 species representing all major clades of anthropoid primates. Contrary to prevailing assumptions, positive selection was not limited to or intensified along the lineage leading to humans. In fact we show that all four loci were subject to positive selection across the anthropoid primate phylogeny. We developed clearly defined hypotheses to explicitly test if selection on these loci was associated with the evolution of brain size. We found positive relationships between both CDK5RAP2 and ASPM and neonatal brain mass and somewhat weaker relationships between these genes and adult brain size. In contrast, there is no evidence linking CENPJ and MCPH1 to brain size evolution. The stronger association of ASPM and CDK5RAP2 evolution with neonatal brain size than with adult brain size is consistent with these loci having a direct effect on prenatal neuronal proliferation. These results suggest that primate brain size may have at least a partially conserved genetic basis. Our results contradict a previous study that linked adaptive evolution of ASPM to changes in relative cortex size; however, our analysis indicates that this conclusion is not robust. Our finding that the coding regions of two widely expressed loci has experienced pervasive positive selection in relation to a complex, quantitative developmental phenotype provides a notable counterexample to the commonly asserted hypothesis that cis-regulatory regions play a dominant role in phenotypic evolution.

Placentation and maternal investment in mammals.

The mammalian placenta exhibits striking interspecific morphological variation, yet the implications of such diversity for reproductive strategies and fetal development remain obscure. More invasive hemochorial placentas, in which fetal tissues directly contact the maternal blood supply, are believed to facilitate nutrient transfer, resulting in higher fetal growth rates, and to be a state of relative fetal advantage in the evolution of maternal-offspring conflict. The extent of interdigitation between maternal and fetal tissues has received less attention than invasiveness but is also potentially important because it influences the surface area for exchange. We show that although increased placental invasiveness and interdigitation are both associated with shorter gestations, interdigitation is the key variable. Gestation times associated with highly interdigitated labyrinthine placentas are 44% of those associated with less interdigitated villous and trabecular placentas. There is, however, no relationship between placental traits and neonatal body and brain size. Hence, species with more interdigitated placentas produce neonates of similar body and brain size but in less than half the time. We suggest that the effects of placental interdigitation on growth rates and the way that these are traded off against gestation length may be promising avenues for understanding the evolutionary dynamics of parent-offspring conflict.

Phylogeny and metabolic scaling in mammals.

The scaling of metabolic rates to body size is widely considered to be of great biological and ecological importance, and much attention has been devoted to determining its theoretical and empirical value. Most debate centers on whether the underlying power law describing metabolic rates is 2/3 (as predicted by scaling of surface area/volume relationships) or 3/4 ("Kleiber's law"). Although recent evidence suggests that empirically derived exponents vary among clades with radically different metabolic strategies, such as ectotherms and endotherms, models, such as the metabolic theory of ecology, depend on the assumption that there is at least a predominant, if not universal, metabolic scaling exponent. Most analyses claimed to support the predictions of general models, however, failed to control for phylogeny. We used phylogenetic generalized least-squares models to estimate allometric slopes for both basal metabolic rate (BMR) and field metabolic rate (FMR) in mammals. Metabolic rate scaling conformed to no single theoretical prediction, but varied significantly among phylogenetic lineages. In some lineages we found a 3/4 exponent, in others a 2/3 exponent, and in yet others exponents differed significantly from both theoretical values. Analysis of the phylogenetic signal in the data indicated that the assumptions of neither species-level analysis nor independent contrasts were met. Analyses that assumed no phylogenetic signal in the data (species-level analysis) or a strong phylogenetic signal (independent contrasts), therefore, returned estimates of allometric slopes that were erroneous in 30% and 50% of cases, respectively. Hence, quantitative estimation of the phylogenetic signal is essential for determining scaling exponents. The lack of evidence for a predominant scaling exponent in these analyses suggests that general models of metabolic scaling, and macro-ecological theories that depend on them, have little explanatory power.

Reconstructing the ups and downs of primate brain evolution: implications for adaptive hypotheses and Homo floresiensis.

BACKGROUND: Brain size is a key adaptive trait. It is often assumed that increasing brain size was a general evolutionary trend in primates, yet recent fossil discoveries have documented brain size decreases in some lineages, raising the question of how general a trend there was for brains to increase in mass over evolutionary time. We present the first systematic phylogenetic analysis designed to answer this question. RESULTS: We performed ancestral state reconstructions of three traits (absolute brain mass, absolute body mass, relative brain mass) using 37 extant and 23 extinct primate species and three approaches to ancestral state reconstruction: parsimony, maximum likelihood and Bayesian Markov-chain Monte Carlo. Both absolute and relative brain mass generally increased over evolutionary time, but body mass did not. Nevertheless both absolute and relative brain mass decreased along several branches. Applying these results to the contentious case of Homo floresiensis, we find a number of scenarios under which the proposed evolution of Homo floresiensis' small brain appears to be consistent with patterns observed along other lineages, dependent on body mass and phylogenetic position. CONCLUSIONS: Our results confirm that brain expansion began early in primate evolution and show that increases occurred in all major clades. Only in terms of an increase in absolute mass does the human lineage appear particularly striking, with both the rate of proportional change in mass and relative brain size having episodes of greater expansion elsewhere on the primate phylogeny. However, decreases in brain mass also occurred along branches in all major clades, and we conclude that, while selection has acted to enlarge primate brains, in some lineages this trend has been reversed. Further analyses of the phylogenetic position of Homo floresiensis and better body mass estimates are required to confirm the plausibility of the evolution of its small brain mass. We find that for our dataset the Bayesian analysis for ancestral state reconstruction is least affected by inclusion of fossil data suggesting that this approach might be preferable for future studies on other taxa with a poor fossil record.