Laboratory maintenance does not alter ecological and physiological patterns among species: a Drosophila case study

Large comparative studies in animal ecology, physiology and evolution often use animals reared in the laboratory for many generations; however, the relevance of these studies hinges on the assumption that laboratory populations are still representative for their wild living conspecifics. In this study, we investigate whether laboratory‐maintained and freshly collected animal populations are fundamentally different and whether data from laboratory‐maintained animals are valid to use in large comparative investigations of ecological and physiological patterns. Here, we obtained nine species of Drosophila with paired populations of laboratory‐maintained and freshly collected flies. These species, representing a range of ecotypes, were assayed for four stress‐tolerance, two body‐size traits and six life‐history traits. For all of these traits, we observed small differences in species‐specific comparisons between field and laboratory populations; however, these differences were unsystematic and laboratory maintenance did not eclipse fundamental species characteristics. To investigate whether laboratory maintenance influence the general patterns in comparative studies, we correlated stress tolerance and life‐history traits with environmental traits for the laboratory‐maintained and freshly collected populations. Based on this analysis, we found that the comparative physiological and ecological trait correlations are similar irrespective of provenience. This finding is important for comparative biology in general because it validates comparative meta‐analyses based on laboratory‐maintained populations.     

Inferring maximum lifespan from maximum recorded longevity in the wild carries substantial risk of estimation bias

When comparing lifespan (longevity) between species, it is common practice to take the maximum recorded longevity value within each species as a proxy of maximum lifespan. Whether maximum recorded longevity is a reliable proxy of species' maximum longevity remains unclear. Some researchers correct for previously documented life history correlates of maximum recorded longevity before analysing new predictors of lifespan across species in the context of their current, specific hypotheses. At present there is no certainty that all relevant statistical, phenotypic, or ecological biases are accounted for by such corrective measures. Here, we employ Monte Carlo simulation to investigate the effect of differences in recapture numbers, recapture types (the point in life at which individuals are initially captured or recaptured), and actuarial population decay structure of simulated species on their maximum recorded longevities. We show that maximum recorded longevities differ in response to all three of these variables, as well as all of their two‐ and three‐way interactions. We then investigate empirical avian band‐recapture data for evidence of biases caused by recapture number and recapture type, predicted by the Monte Carlo analysis, and confirm the predicted biases as major sources of variance. Finally, we investigate the relationship between recapture type, recapture number, and a selection of ecological and life‐history variables previously documented to correlate with maximum recorded longevity, and find significant correlations between the biasing variables and those published correlates. Our results call into question the validity of using maximum recorded longevity as a proxy for different species' maximum longevities in comparative studies investigating the evolution of lifespan.     

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

When novel sources of ecological opportunity are available, physiological innovations can trigger adaptive radiations. This could be the case of yeasts (Saccharomycotina), in which an evolutionary novelty is represented by the capacity to exploit simple sugars from fruits (fermentation). During adaptive radiations, diversification and morphological evolution are predicted to slow‐down after early bursts of diversification. Here, we performed the first comparative phylogenetic analysis in yeasts, testing the “early burst” prediction on species diversification and also on traits of putative ecological relevance (cell‐size and fermentation versatility). We found that speciation rates are constant during the time‐range we considered (ca., 150 millions of years). Phylogenetic signal of both traits was significant (but lower for cell‐size), suggesting that lineages resemble each other in trait‐values. Disparity analysis suggested accelerated evolution (diversification in trait values above Brownian Motion expectations) in cell‐size. We also found a significant phylogenetic regression between cell‐size and fermentation versatility (R² = 0.10), which suggests correlated evolution between both traits. Overall, our results do not support the early burst prediction both in species and traits, but suggest a number of interesting evolutionary patterns, that warrant further exploration. For instance, we show that the Whole Genomic Duplication that affected a whole clade of yeasts, does not seems to have a statistically detectable phenotypic effect at our level of analysis. In this regard, further studies of fermentation under common‐garden conditions combined with comparative analyses are warranted.     

Woody species in resource‐rich microrefugia of granite outcrops display unique functional signatures

Refugia are key environments in biogeography and conservation. Because of their unique eco‐evolutionary formation and functioning, they should display distinct functional trait signatures. However, comparative trait‐based studies of plants in refugia and non‐refugia are lacking. Here, we provide a comparison between resource‐rich (putative microrefugia for species preferring mesic habitats under increasing aridity) and resource‐impoverished woodlands (non‐refugia) around two granite outcrops in south‐western Australia. We measured and compared six functional traits (bark thickness, foliar δ¹³C, foliar C:N, leaf dry matter content, plant height, specific leaf area) in four woody species. We performed multiple‐trait, multiple‐species and single‐trait, within‐species analyses to test whether plants in resource‐rich habitats were functionally distinct and more diverse than those in the surrounding resource‐impoverished woodlands. We found that species in resource‐rich woodlands occupied larger and distinct multiple‐trait functional spaces and showed distinct single‐trait values (for specific leaf area and bark thickness). This suggests that plants in resource‐rich woodlands can deploy unique and more diverse ecological strategies, potentially making these putative microrefugia more resilient to environmental changes. These findings suggest that species in microrefugia may be characterised by unique functional signatures, illustrating the utility of comparative trait‐based approaches to improve understanding of the functioning of refugia.     

Dispersal capacity explains the evolution of lifespan variability

The evolutionary explanation for lifespan variation is still based on the antagonistic pleiotropy hypothesis, which has been challenged by several studies. Alternative models assume the existence of genes that favor aging and group benefits at the expense of reductions in individual lifespans. Here we propose a new model without making such assumptions. It considers that limited dispersal can generate, through reduced gene flow, spatial segregation of individual organisms according to lifespan. Individuals from subpopulations with shorter lifespan could thus resist collapse in a growing population better than individuals from subpopulations with longer lifespan, hence reducing lifespan variability within species. As species that disperse less may form more homogeneous subpopulations regarding lifespan, this may lead to a greater capacity to maximize lifespan that generates viable subpopulations, therefore creating negative associations between dispersal capacity and lifespan across species. We tested our model with individual‐based simulations and a comparative study using empirical data of maximum lifespan and natal dispersal distance in 26 species of birds, controlling for the effects of genetic variability, body size, and phylogeny. Simulations resulted in maximum lifespans arising from lowest dispersal probabilities, and comparative analyses resulted in a negative association between lifespan and natal dispersal distance, thus consistent with our model. Our findings therefore suggest that the evolution of lifespan variability is the result of the ecological process of dispersal.     

Global gradients of avian longevity support the classic evolutionary theory of ageing

Senescence, the process of physiological deterioration associated with growing old, is a shared characteristic of a wide range of animals. Yet, lifespan varies dramatically among species. To explain this variation, the evolutionary theory of ageing has been proposed more than 50 yr ago. Although the theory has been tested experimentally and through comparative analyses, there remains debate whether its fundamental prediction is empirically supported. Here, we use a comprehensive database on avian life history traits to test the evolutionary theory of ageing at a global scale. We show that pronounced geographical gradients of maximum longevity exist, that they are predicted by measures of predator diversity and only partly depend on correlated life‐history traits. The results are consistent with species‐level analyses and can be replicated across bio‐geographical regions. Our analyses suggest that stochastic predation is an important driver of the evolution of lifespan, at least in birds.     

Phylogenetic comparisons of pedestrian locomotion costs: confirmations and new insights

The energetic costs for animals to locomote on land influence many aspects of their ecology. Size accounts for much of the among‐species variation in terrestrial transport costs, but species of similar body size can still exhibit severalfold differences in energy expenditure. We compiled measurements of the (mass‐specific) minimum cost of pedestrian transport (COT_min, mL/kg/m) for 201 species – by far the largest sample to date – and used phylogenetically informed comparative analyses to investigate possible eco‐evolutionary differences in COT_min between various groupings of those species. We investigated number of legs, ectothermy and endothermy, waddling, and nocturnality specifically in lizards. Thus, our study primarily revisited previous theories about variations in COT_min between species, testing them with much more robust analyses. Having accounted for mass, while residual COT_min did not differ between bipedal and other species, specifically waddling bipeds were found to have relatively high COT_min. Furthermore, nocturnal lizards have relatively low COT_min although temperature does not appear to affect COT_min in ectotherms. Previous studies examining across‐species variation in COT_min from a biomechanical perspective show that the differences between waddling birds and nonwaddling species, and between nocturnal lizards and other ecotherms, are likely to be attributable to differences in ground reaction forces, posture, and effective limb length.     

ACCOUNTING FOR RATE VARIATION AMONG LINEAGES IN COMPARATIVE DEMOGRAPHIC ANALYSES

Genetic analyses of contemporary populations can be used to estimate the demographic histories of species within an ecological community. Comparison of these demographic histories can shed light on community responses to past climatic events. However, species experience different rates of molecular evolution, and this presents a major obstacle to comparative demographic analyses. We address this problem by using a Bayesian relaxed‐clock method to estimate the relative evolutionary rates of 22 small mammal taxa distributed across northwestern North America. We found that estimates of the relative molecular substitution rate for each taxon were consistent across the range of sampling schemes that we compared. Using three different reference rates, we rescaled the relative rates so that they could be used to estimate absolute evolutionary timescales. Accounting for rate variation among taxa led to temporal shifts in our skyline‐plot estimates of demographic history, highlighting both uniform and idiosyncratic evolutionary responses to directional climate trends for distinct ecological subsets of the small mammal community. Our approach can be used in evolutionary analyses of populations from multiple species, including comparative demographic studies.     

Correlations between physiology and lifespan--two widely ignored problems with comparative studies

Comparative differences between species provide a powerful source of information that may inform our understanding of the aging process. However, two problems regularly attend such analyses. The co-variation of traits with body mass is frequently ignored, along with the lack of independence of the data due to a shared phylogenetic history. These problems undermine the use of simple correlations between various factors and maximum lifespan potential (MLSP) across different species as evidence that the factors in question have causal effects on aging. Both of these problems have been widely addressed by comparative biologists working in fields other than aging research, and statistical solutions to these issues are available. Using these statistical approaches, of making analyses of residual traits with the effects of body mass removed, and deriving phylogenetically independent contrasts, will allow analyses of the relationships between physiology and maximum lifespan potential to proceed unhindered by these difficulties, potentially leading to many useful insights into the aging process.     

The “unguarded‐X” and the genetic architecture of lifespan: Inbreeding results in a potentially maladaptive sex‐specific reduction of female lifespan in Drosophila melanogaster

Sex differences in ageing and lifespan are ubiquitous in nature. The "unguarded‐X” hypothesis (UXh) suggests they may be partly due to the expression of recessive mutations in the hemizygous sex chromosomes of the heterogametic sex, which could help explain sex‐specific ageing in a broad array of taxa. A prediction central to the UX hypothesis is that inbreeding will decrease the lifespan of the homogametic sex more than the heterogametic sex, because only in the former does inbreeding increase the expression of recessive deleterious mutations. In this study, we test this prediction by examining the effects of inbreeding on the lifespan and fitness of male and female Drosophila melanogaster across different social environments. We found that, across social environments, inbreeding resulted in a greater reduction of female than male lifespan, and that inbreeding effects on fitness did not seem to counterbalance sex‐specific effects on lifespan, suggesting the former are maladaptative. Inter‐ and intra‐sexual correlation analyses also allowed us to identify evidence of an underlying joint genetic architecture for inbreeding effects on lifespan. We discuss these results in light of the UXh and other alternative explanations, and suggest that more attention should be paid to the possibility that the “unguarded‐X” may play an important role in the evolution of sex‐specific lifespan.     

Variation of butterfly diet breadth in relation to host-plant predictability: results from two faunas

Host‐plant data for North American and Australian butterflies were used to test the hypothesis that larval diet breadth increases with decreasing resource predictability (where the latter was estimated by host‐plant growth‐form/duration). For each region in turn we compared the diet breadths of butterflies which utilise herbaceous host‐plants with those of species having woody hosts. For North America alone we also compared the diet breadths of species having annual hosts with those utilising perennial hosts, and the diets of species having herbaceous‐annual hosts with those using woody‐perennial hosts. Studies of diet breadth may be biased by the host taxonomic level which contributes most to the diet index used. For example, the results of analyses which employ indices based on numbers of families of hosts utilised may differ from those using indices based on counts of host species or genera. To investigate this potential problem we performed cross‐species analyses where diet breadth was defined in turn as the number of host species, genera, or families eaten. We found that using different taxonomic levels did give inconsistent results. To avoid this we employed phylogenetic diet breadth indices in comparative analyses of Independent Contrasts. The former incorporate information from the whole of the host‐plant phylogeny, whilst the comparative method eliminates any confounding effects of butterfly phylogeny. The results indicated that there is a phylogenetic component to butterfly diet breadth. They also largely differed from those of the cross‐species investigations, although there were similarities (i.e. results differed between regions and varied according to whether the whole fauna or just endemics were investigated). Our results suggested that in both regions, non‐endemics which feed on herbaceous plants have wider diet breadths than non‐endemics which utilise woody hosts. However, we found no consistent evidence that the diet breadths of endemics increase with decreasing resource predictability (as estimated here).     

The human post‐fertile lifespan in comparative evolutionary context

There persist two widely held but mutually inconsistent views on the evolution of post‐fertile lifespan of human females. The first, prevalent within anthropology, sees post‐fertile lifespan (PFLS) in the light of adaptive processes, focusing on the social and economic habits of humans that selected for a lengthy PFLS. 1 - 3 This view rests on the assumption that human PFLS is distinct from that of other species, and focuses on quantifying the selective causes and consequences of that difference. The second view, prevalent within gerontology and comparative biology, emphasizes that PFLS is a phylogenetically widespread trait 4 - 6 or that human PFLS is predictable based on life‐history allometries. 7 In this view, human PFLS is part of a broad cross‐species pattern and its genesis cannot, therefore, rely on human‐specific traits. Those who advocate the second view have questioned the “special pleading” for human specific explanations of PFLS, 4 and have argued that human PFLS is quantitatively greater but not qualitatively different than PFLS in many other animals. 5 , 8 Papers asking whether human PFLS is explained by the importance of mothers more than grandmothers, whether paternal or maternal grandparents have more of an effect on child survival, or who is providing the excess calories are associated with the first view that assumes the need to explain the existence of human PFLS on the basis of a uniquely human socioecology. Anthropologists largely see human PFLS as derived, while comparative gerontologists point to evidence that it is one instance of a ubiquitous cross‐species pattern. The two groups generally occupy non‐overlapping research circles, in terms of conferences and journals, and therefore interact little enough to largely avoid the need to reconcile their views, allowing the persistence of misconceptions in each field. Our goal is to identify and address the most important of these misconceptions and thereby make clear that both of these seemingly incongruent views contain valid points. We argue that two distinct but related traits have been lumped together under the same concept of “post‐reproductive lifespan,” one (post‐fertile viability) that is tremendously widespread and another (a post‐fertile life stage) that is derived to hominins, and that the differences and connections between these two traits are necessary for understanding human life‐history evolution.     

Assessing the impacts of imperfect detection on estimates of diversity and community structure through multispecies occupancy modeling

Detecting all species in a given survey is challenging, regardless of sampling effort. This issue, more commonly known as imperfect detection, can have negative impacts on data quality and interpretation, most notably leading to false absences for rare or difficult‐to‐detect species. It is important that this issue be addressed, as estimates of species richness are critical to many areas of ecological research and management. In this study, we set out to determine the impacts of imperfect detection, and decisions about thresholds for inclusion in occupancy, on estimates of species richness and community structure. We collected data from a stream fish assemblage in Algonquin Provincial Park to be used as a representation of ecological communities. We then used multispecies occupancy modeling to estimate species‐specific occurrence probabilities while accounting for imperfect detection, thus creating a more informed dataset. This dataset was then compared to the original to see where differences occurred. In our analyses, we demonstrated that imperfect detection can lead to large changes in estimates of species richness at the site level and summarized differences in the community structure and sampling locations, represented through correspondence analyses.     

Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta‐analytic review

Comparative analyses aim to explain interspecific variation in phenotype among taxa. In this context, phylogenetic approaches are generally applied to control for similarity due to common descent, because such phylogenetic relationships can produce spurious similarity in phenotypes (known as phylogenetic inertia or bias). On the other hand, these analyses largely ignore potential biases due to within‐species variation. Phylogenetic comparative studies inherently assume that species‐specific means from intraspecific samples of modest sample size are biologically meaningful. However, within‐species variation is often significant, because measurement errors, within‐ and between‐individual variation, seasonal fluctuations, and differences among populations can all reduce the repeatability of a trait. Although simulations revealed that low repeatability can increase the type I error in a phylogenetic study, researchers only exercise great care in accounting for similarity in phenotype due to common phylogenetic descent, while problems posed by intraspecific variation are usually neglected. A meta‐analysis of 194 comparative analyses all adjusting for similarity due to common phylogenetic descent revealed that only a few studies reported intraspecific repeatabilities, and hardly any considered or partially dealt with errors arising from intraspecific variation. This is intriguing, because the meta‐analytic data suggest that the effect of heterogeneous sampling can be as important as phylogenetic bias, and thus they should be equally controlled in comparative studies. We provide recommendations about how to handle such effects of heterogeneous sampling.     

COMPARATIVE ANALYSES OF SEX‐RATIO VARIATION IN DIOECIOUS FLOWERING PLANTS

Dioecious plant species commonly exhibit deviations from the equilibrium expectation of 1:1 sex ratio, but the mechanisms governing this variation are poorly understood. Here, we use comparative analyses of 243 species, representing 123 genera and 61 families to investigate ecological and genetic correlates of variation in the operational (flowering) sex ratio. After controlling for phylogenetic nonindependence, we examined the influence of growth form, clonality, fleshy fruits, pollen and seed dispersal vector, and the possession of sex chromosomes on sex‐ratio variation. Male‐biased flowering sex ratios were twice as common as female‐biased ratios. Male bias was associated with long‐lived growth forms (e.g., trees) and biotic seed dispersal and fleshy fruits, whereas female bias was associated with clonality, especially for herbaceous species, and abiotic pollen dispersal. Female bias occurred in species with sex chromosomes and there was some evidence for a greater degree of bias in those with heteromorphic sex chromosomes. Although the role of interactions among these correlates require further study, our results indicate that sex‐based differences in costs of reproduction, pollen and seed dispersal mechanisms and sex chromosomes can each play important roles in affecting flowering sex ratios in dioecious plants.     

Exploring the predictive performance of several temperature measurements on Neotropical dung beetle assemblages: Methodological implications

Basic characteristics of species assemblages are frequently related to temperature variables recorded at a coarse‐grained scale. In this study, 15 min instant‐measurements of environmental and soil temperatures were recorded during 1 year in six Atlantic Forest sites of southern Brazil, ranging from 250 to 1,630 m a.s.l. These measurements were used to examine the comparative explanatory capacity of several temperature variables in predicting species richness and total or specific variations of dung beetle abundance. The results suggest that temperature measurements obtained during the survey period have the highest explanatory capacity. Furthermore, average temperature values seem to have a relatively higher explanatory capacity than absolute minimum or maximum values reflecting extreme conditions. In general, there is no rule in selecting a temperature variable when the objective involves explaining the variation in species abundances. Both soil and air variables can have similar explanatory capacities. The present results should be considered when designing future ecological studies in Neotropical conditions.     

THE QUANTITATIVE ASSESSMENT OF PHYLOGENETIC CONSTRAINTS IN COMPARATIVE ANALYSES: SEXUAL DIMORPHISM IN BODY WEIGHT AMONG PRIMATES

We have presented a formal model for the quantitative analysis of phylogenetic and specific effects on the distribution of trait values among species. Total trait values are divided into phylogenetic values, inherited from an ancestral species, and specific values, the result of independent evolution. This allows a quantitative assessment of the strength of the phylogenetic inertia, or burden, displayed by a character in a lineage, so that questions concerning the relative importance of phylogenetic constraints in evolution can be answered. The separation of phylogenetic from specific effects proposed here also allows phylogenetic factors to be explicitly included in cross-species comparative analyses of adaptation. This solves a long-standing problem in evolutionary comparative studies. Only species' specific values can provide information concerning the independent evolution of characters in a set of related species. Therefore, only correlations among specific values for traits may be used as evidence for adaptation in cross-species comparative analyses. The phylogenetic autocorrelation model was applied to a comparative analysis of the determinants of sexual dimorphism in weight among 44 primate species. In addition to sexual dimorphism in weight, mating system, habitat, diet, and size (weight itself) were included in the analysis. All of the traits, except diet, were substantially influenced by phylogenetic inertia. The comparative analysis of the determinants of sexual dimorphism in weight indicates that 50% of the variation among primate species is due to phylogeny. Size, or scaling, could account for a total of 36% of the variance, making it almost as important as phylogeny in determining the level of dimorphism displayed by a species. Habitat, mating system, and diet follow, accounting for minor amounts of variation. Thus, in attempting to explain why a particular modern primate species is very dimorphic compared to other primates, we would say first because its ancestor was more dimorphic than average, second because it is a relatively large species, and third because it is terrestrial, polygynous, and folivorous.