The costs and benefits of paternal care in fish: a meta-analysis.

Male-only parental care, while rare in most animals, is a widespread strategy within teleost fish. The costs and benefits to males of acting as sole carer are highly variable among fish species making it challenging to determine the selective pressures driving the evolution of male-only care to such a high prevalence. We conducted a phylogenetic meta-analysis to examine the costs and benefits of paternal care across fish species. We found no evidence that providing care negatively affects male condition. In contrast with other taxa, we also found limited evidence that male care has evolved as a strategy to improve offspring survival. Instead, we found that males already caring for a brood are preferred by females and that this preference is strongest in those species in which males work harder to care for larger broods. Thus, in fish, investment in offspring care does not constrain a male's mating success but rather augments it, suggesting that the relatively high prevalence of male-only care in fish may be in part explained by sexual selection through female preference for caring males.

Temporal and spatial limitations in global surveillance for bat filoviruses and henipaviruses.

Sampling reservoir hosts over time and space is critical to detect epizootics, predict spillover and design interventions. However, because sampling is logistically difficult and expensive, researchers rarely perform spatio-temporal sampling of many reservoir hosts. Bats are reservoirs of many virulent zoonotic pathogens such as filoviruses and henipaviruses, yet the highly mobile nature of these animals has limited optimal sampling of bat populations. To quantify the frequency of temporal sampling and to characterize the geographical scope of bat virus research, we here collated data on filovirus and henipavirus prevalence and seroprevalence in wild bats. We used a phylogenetically controlled meta-analysis to next assess temporal and spatial variation in bat virus detection estimates. Our analysis shows that only one in four bat virus studies report data longitudinally, that sampling efforts cluster geographically (e.g. filovirus data are available across much of Africa and Asia but are absent from Latin America and Oceania), and that sampling designs and reporting practices may affect some viral detection estimates (e.g. filovirus seroprevalence). Within the limited number of longitudinal bat virus studies, we observed high heterogeneity in viral detection estimates that in turn reflected both spatial and temporal variation. This suggests that spatio-temporal sampling designs are important to understand how zoonotic viruses are maintained and spread within and across wild bat populations, which in turn could help predict and preempt risks of zoonotic viral spillover.

On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis.

Body condition metrics are widely used to infer animal health and to assess costs of parasite infection. Since parasites harm their hosts, ecologists might expect negative relationships between infection and condition in wildlife, but this assumption is challenged by studies showing positive or null condition-infection relationships. Here, we outline common condition metrics used by ecologists in studies of parasitism, and consider mechanisms that cause negative, positive, and null condition-infection relationships in wildlife systems. We then perform a meta-analysis of 553 condition-infection relationships from 187 peer-reviewed studies of animal hosts, analysing observational and experimental records separately, and noting whether authors measured binary infection status or intensity. Our analysis finds substantial heterogeneity in the strength and direction of condition-infection relationships, a small, negative average effect size that is stronger in experimental studies, and evidence for publication bias towards negative relationships. The strongest predictors of variation in study outcomes are host thermoregulation and the methods used to evaluate body condition. We recommend that studies aiming to assess parasite impacts on body condition should consider host-parasite biology, choose condition measures that can change during the course of infection, and employ longitudinal surveys or manipulate infection status when feasible.

Using host species traits to understand the consequences of resource provisioning for host-parasite interactions.

Supplemental food provided to wildlife by human activities can be more abundant and predictable than natural resources, and subsequent changes in wildlife ecology can have profound impacts on host-parasite interactions. Identifying traits of species associated with increases or decreases in infection outcomes with resource provisioning could improve assessments of wildlife most prone to disease risks in changing environments. We conducted a phylogenetic meta-analysis of 342 host-parasite interactions across 56 wildlife species and three broad taxonomic groups of parasites to identify host-level traits that influence whether provisioning is associated with increases or decreases in infection. We predicted dietary generalists that capitalize on novel food would show greater infection in provisioned habitats owing to population growth and food-borne exposure to contaminants and parasite infectious stages. Similarly, species with fast life histories could experience stronger demographic and immunological benefits from provisioning that affect parasite transmission. We also predicted that wide-ranging and migratory behaviours could increase infection risks with provisioning if concentrated and non-seasonal foods promote dense aggregations that increase exposure to parasites. We found that provisioning increased infection with bacteria, viruses, fungi and protozoa (i.e. microparasites) most for wide-ranging, dietary generalist host species. Effect sizes for ectoparasites were also highest for host species with large home ranges but were instead lowest for dietary generalists. In contrast, the type of provisioning was a stronger correlate of infection outcomes for helminths than host species traits. Our analysis highlights host traits related to movement and feeding behaviour as important determinants of whether species experience greater infection with supplemental feeding. These results could help prioritize monitoring wildlife with particular trait profiles in anthropogenic habitats to reduce infectious disease risks in provisioned populations.

Hybridisation is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridisation-invasion hypothesis.

The hypothesis that interspecific hybridisation promotes invasiveness has received much recent attention, but tests of the hypothesis can suffer from important limitations. Here, we provide the first systematic review of studies experimentally testing the hybridisation-invasion (H-I) hypothesis in plants, animals and fungi. We identified 72 hybrid systems for which hybridisation has been putatively associated with invasiveness, weediness or range expansion. Within this group, 15 systems (comprising 34 studies) experimentally tested performance of hybrids vs. their parental species and met our other criteria. Both phylogenetic and non-phylogenetic meta-analyses demonstrated that wild hybrids were significantly more fecund and larger than their parental taxa, but did not differ in survival. Resynthesised hybrids (which typically represent earlier generations than do wild hybrids) did not consistently differ from parental species in fecundity, survival or size. Using meta-regression, we found that fecundity increased (but survival decreased) with generation in resynthesised hybrids, suggesting that natural selection can play an important role in shaping hybrid performance - and thus invasiveness - over time. We conclude that the available evidence supports the H-I hypothesis, with the caveat that our results are clearly driven by tests in plants, which are more numerous than tests in animals and fungi.

All eggs are made equal: meta-analysis of egg sexual size dimorphism in birds.

Sex-biased resource allocation in avian eggs has gained increasing interest. The adaptive explanations of such allocation are often related to life-history strategies of the studied species. In some species, egg sexual size dimorphism (SSD) was suggested to promote future size differences between adults of each sex. In other species, egg SSD was invoked as an adaptive means by which a mother balances sex-specific nestling mortality. According to the first scenario, mothers should produce bigger eggs for the bigger sex, thus across species, adult SSD should be a significant positive predictor of egg SSD. Under the second scenario, mothers should produce bigger eggs for the smaller sex. If different species use contrasting strategies, then a universal expectation is that there should be a significant relationship between the magnitude of adult SSD and the magnitude of egg SSD, irrespective of the direction of those differences. Our aim was to examine whether the direction of egg SSD is predicted by the direction of adult SSD or whether degree of egg SSD is related to degree of adult SSD. To answer that question, we performed meta-analysis of 63 studies, which included information on egg SSD of 65 effect sizes from 51 avian species. We found that across species, adult SSD does not predict egg SSD. More importantly, the observed variation in effect sizes in our data set was largely explained by sampling error (variance). Although adult SSD is undoubtedly a prominent feature of birds, there is little evidence for egg SSD across avian species.

Does moonlight increase predation risk? Meta-analysis reveals divergent responses of nocturnal mammals to lunar cycles.

The risk of predation strongly affects mammalian population dynamics and community interactions. Bright moonlight is widely believed to increase predation risk for nocturnal mammals by increasing the ability of predators to detect prey, but the potential for moonlight to increase detection of predators and the foraging efficiency of prey has largely been ignored. Studies have reported highly variable responses to moonlight among species, calling into question the assumption that moonlight increases risk. Here, we conducted a quantitative meta-analysis examining the effects of moonlight on the activity of 59 nocturnal mammal species to test the assumption that moonlight increases predation risk. We examined patterns of lunarphilia and lunarphobia across species in relation to factors such as trophic level, habitat cover preference and visual acuity. Across all species included in the meta-analysis, moonlight suppressed activity. The magnitude of suppression was similar to the presence of a predator in experimental studies of foraging rodents (13.6% and 18.7% suppression, respectively). Contrary to the expectation that moonlight increases predation risk for all prey species, however, moonlight effects were not clearly related to trophic level and were better explained by phylogenetic relatedness, visual acuity and habitat cover. Moonlight increased the activity of prey species that use vision as their primary sensory system and suppressed the activity of species that primarily use other senses (e.g. olfaction, echolocation), and suppression was strongest in open habitat types. Strong taxonomic patterns underlay these relationships: moonlight tended to increase primate activity, whereas it tended to suppress the activity of rodents, lagomorphs, bats and carnivores. These results indicate that visual acuity and habitat cover jointly moderate the effect of moonlight on predation risk, whereas trophic position has little effect. While the net effect of moonlight appears to increase predation risk for most nocturnal mammals, our results highlight the importance of sensory systems and phylogenetic history in determining the level of risk.

Phylogenetic meta-analysis reveals system-specific behavioural type-behavioural predictability correlations.

The biological significance of behavioural predictability (environment-independent within-individual behavioural variation) became accepted recently as an important part of an individual's behavioural strategy besides behavioural type (individual mean behaviour). However, we do not know how behavioural type and predictability evolve. Here, we tested different evolutionary scenarios: (i) the two traits evolve independently (lack of correlations) and (ii) the two traits' evolution is constrained (abundant correlations) due to either (ii/a) proximate constraints (direction of correlations is similar) or (ii/b) local adaptations (direction of correlations is variable). We applied a set of phylogenetic meta-analyses based on 93 effect sizes across 44 vertebrate and invertebrate species, focusing on activity and risk-taking. The general correlation between behavioural type and predictability did not differ from zero. Effect sizes for correlations showed considerable heterogeneity, with both negative and positive correlations occurring. The overall absolute (unsigned) effect size was high (Zr = 0.58), and significantly exceeded the null expectation based on randomized data. Our results support the adaptive scenario: correlations between behavioural type and predictability are abundant in nature, but their direction is variable. We suggest that the evolution of these behavioural components might be constrained in a system-specific way.

Magnitude and direction of parasite-induced phenotypic alterations: a meta-analysis in acanthocephalans.

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta-analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite-induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro-habitat and the anti-predation behaviour of infected hosts, and by promoting energy-saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host-parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of parasites.

Megafauna Seed Dispersal in the Neotropics: A Meta-Analysis Shows No Genetic Signal of Loss of Long-Distance Seed Dispersal.

Restricted gene flow may lead to the loss of genetic diversity and higher genetic differentiation among populations, but the genetic consequences of megafauna extinction for plant populations still remain to be assessed. We performed a phylogenetic-independent meta-analysis across 102 Neotropical plants to test the hypothesis that plant species with megafaunal seed dispersal syndrome have a lower genetic diversity and a higher genetic differentiation than those without it. We classified as megafauna-dependent plant species those that potentially relied only on megafauna to seed dispersal, and as megafauna-independent those that relied on megafauna and other seed dispersers. Our data comprised 98 studies using microsatellite markers. We found no statistical difference in genetic diversity and differentiation between plants with megafauna and non-megafauna seed dispersal syndrome, although the statistical power to detect differences in genetic differentiation was low. Moreover, we found no statistical difference between megafauna-dependent and megafauna-independent plant species. We then used generalized linear mixed models and phylogenetic generalized least square models to investigate the effects of megafaunal seed dispersal syndromes and reproductive traits on variation in genetic diversity and genetic differentiation. We found no effect of megafaunal syndrome, rather, reproductive traits, such as pollination mode, mating, and breeding systems, showed significant effects. Our findings show that the genetic studies of Neotropical plants performed so far show no difference in genetic diversity and differentiation in plants with megafaunal compared to those with non-megafaunal seed dispersal syndromes. Our results also provide evidence pointing out that plant species with megafaunal seed dispersal syndromes may have used different strategies to counterbalance the extinction of their mutualistic megafauna dispersers, such as the dispersal by extant mammals that may promote long-distance seed dispersal. Our results also reinforce the importance of pollination to long-distance gene flow in Neotropical plants.

Biomass Allocation of Stoloniferous and Rhizomatous Plant in Response to Resource Availability: A Phylogenetic Meta-Analysis.

Resource allocation to different functions is central in life-history theory. Plasticity of functional traits allows clonal plants to regulate their resource allocation to meet changing environments. In this study, biomass allocation traits of clonal plants were categorized into absolute biomass for vegetative growth vs. for reproduction, and their relative ratios based on a data set including 115 species and derived from 139 published literatures. We examined general pattern of biomass allocation of clonal plants in response to availabilities of resource (e.g., light, nutrients, and water) using phylogenetic meta-analysis. We also tested whether the pattern differed among clonal organ types (stolon vs. rhizome). Overall, we found that stoloniferous plants were more sensitive to light intensity than rhizomatous plants, preferentially allocating biomass to vegetative growth, aboveground part and clonal reproduction under shaded conditions. Under nutrient- and water-poor condition, rhizomatous plants were constrained more by ontogeny than by resource availability, preferentially allocating biomass to belowground part. Biomass allocation between belowground and aboveground part of clonal plants generally supported the optimal allocation theory. No general pattern of trade-off was found between growth and reproduction, and neither between sexual and clonal reproduction. Using phylogenetic meta-analysis can avoid possible confounding effects of phylogeny on the results. Our results shown the optimal allocation theory explained a general trend, which the clonal plants are able to plastically regulate their biomass allocation, to cope with changing resource availability, at least in stoloniferous and rhizomatous plants.

Fifty years of chasing lizards: new insights advance optimal escape theory.

Systematic reviews and meta-analyses often examine data from diverse taxa to identify general patterns of effect sizes. Meta-analyses that focus on identifying generalisations in a single taxon are also valuable because species in a taxon are more likely to share similar unique constraints. We conducted a comprehensive phylogenetic meta-analysis of flight initiation distance in lizards. Flight initiation distance (FID) is a common metric used to quantify risk-taking and has previously been shown to reflect adaptive decision-making. The past decade has seen an explosion of studies focused on quantifying FID in lizards, and, because lizards occur in a wide range of habitats, are ecologically diverse, and are typically smaller and differ physiologically from the better studied mammals and birds, they are worthy of detailed examination. We found that variables that reflect the costs or benefits of flight (being engaged in social interactions, having food available) as well as certain predator effects (predator size and approach speed) had large effects on FID in the directions predicted by optimal escape theory. Variables that were associated with morphology (with the exception of crypsis) and physiology had relatively small effects, whereas habitat selection factors typically had moderate to large effect sizes. Lizards, like other taxa, are very sensitive to the costs of flight.