Fast-slow continuum and reproductive strategies structure plant life-history variation worldwide.

The identification of patterns in life-history strategies across the tree of life is essential to our prediction of population persistence, extinction, and diversification. Plants exhibit a wide range of patterns of longevity, growth, and reproduction, but the general determinants of this enormous variation in life history are poorly understood. We use demographic data from 418 plant species in the wild, from annual herbs to supercentennial trees, to examine how growth form, habitat, and phylogenetic relationships structure plant life histories and to develop a framework to predict population performance. We show that 55% of the variation in plant life-history strategies is adequately characterized using two independent axes: the fast-slow continuum, including fast-growing, short-lived plant species at one end and slow-growing, long-lived species at the other, and a reproductive strategy axis, with highly reproductive, iteroparous species at one extreme and poorly reproductive, semelparous plants with frequent shrinkage at the other. Our findings remain consistent across major habitats and are minimally affected by plant growth form and phylogenetic ancestry, suggesting that the relative independence of the fast-slow and reproduction strategy axes is general in the plant kingdom. Our findings have similarities with how life-history strategies are structured in mammals, birds, and reptiles. The position of plant species populations in the 2D space produced by both axes predicts their rate of recovery from disturbances and population growth rate. This life-history framework may complement trait-based frameworks on leaf and wood economics; together these frameworks may allow prediction of responses of plants to anthropogenic disturbances and changing environments.

Transcending data gaps: a framework to reduce inferential errors in ecological analyses.

The analysis of functional diversity (FD) has gained increasing importance due to its generality and utility in ecology. In particular, patterns in the spatial distribution and temporal change of FD are being used to predict locations and functional groups that are immediately vulnerable to global changes. A major impediment to the accurate measurement of FD is the pervasiveness of missing data in trait datasets. While such prevalent data gaps can engender misleading inferences in FD analyses, we currently lack any practical guide to handle missing data in trait datasets. Here, we identify significant mismatches between true FD and values derived from datasets that contain missing data. We demonstrate that imputing missing data with a phylogeny-informed approach reduces the risk of misinterpretation of FD patterns, and provides baseline information against which central questions in ecology can be evaluated.

Extinct or still out there? Disentangling influences on extinction and rediscovery helps to clarify the fate of species on the edge.

Each year, two or three species that had been considered to be extinct are rediscovered. Uncertainty about whether or not a species is extinct is common, because rare and highly threatened species are difficult to detect. Biological traits such as body size and range size are expected to be associated with extinction. However, these traits, together with the intensity of search effort, might influence the probability of detection and extinction differently. This makes statistical analysis of extinction and rediscovery challenging. Here, we use a variant of survival analysis known as cure rate modelling to differentiate factors that influence rediscovery from those that influence extinction. We analyse a global data set of 99 mammals that have been categorized as extinct or possibly extinct. We estimate the probability that each of these mammals is still extant and thus estimate the proportion of missing (presumed extinct) mammals that are incorrectly assigned extinction. We find that body mass and population density are predictors of extinction, and body mass and search effort predict rediscovery. In mammals, extinction rate increases with body mass and population density, and these traits act synergistically to greatly elevate extinction rate in large species that also occurred in formerly dense populations. However, when they remain extant, larger-bodied missing species are rediscovered sooner than smaller species. Greater search effort increases the probability of rediscovery in larger species of missing mammals, but has a minimal effect on small species, which take longer to be rediscovered, if extant. By separating the effects of species characteristics on extinction and detection, and using models with the assumption that a proportion of missing species will never be rediscovered, our new approach provides estimates of extinction probability in species with few observation records and scant ecological information.

Sperm competition drives the evolution of suicidal reproduction in mammals.

Suicidal reproduction (semelparity) has evolved in only four genera of mammals. In these insectivorous marsupials, all males die after mating, when failure of the corticosteroid feedback mechanism elevates stress hormone levels during the mating season and causes lethal immune system collapse (die-off). We quantitatively test and resolve the evolutionary causes of this surprising and extreme life history strategy. We show that as marsupial predators in Australia, South America, and Papua New Guinea diversified into higher latitudes, seasonal predictability in abundance of their arthropod prey increased in multiple habitats. More-predictable prey peaks were associated with shorter annual breeding seasons, consistent with the suggestion that females accrue fitness benefits by timing peak energy demands of reproduction to coincide with maximum food abundance. We demonstrate that short mating seasons intensified reproductive competition between males, increasing male energy investment in copulations and reducing male postmating survival. However, predictability of annual prey cycles alone does not explain suicidal reproduction, because unlike insect abundance, peak ovulation dates in semelparous species are often synchronized to the day among years, triggered by a species-specific rate of change of photoperiod. Among species with low postmating male survival, we show that those with suicidal reproduction have shorter mating seasons and larger testes relative to body size. This indicates that lethal effort is adaptive in males because females escalate sperm competition by further shortening and synchronizing the annual mating period and mating promiscuously. We conclude that precopulatory sexual selection by females favored the evolution of suicidal reproduction in mammals.

The evolution of relative brain size in marsupials is energetically constrained but not driven by behavioral complexity.

Evolutionary increases in mammalian brain size relative to body size are energetically costly but are also thought to confer selective advantages by permitting the evolution of cognitively complex behaviors. However, many suggested associations between brain size and specific behaviors - particularly related to social complexity - are possibly confounded by the reproductive diversity of placental mammals, whose brain size evolution is the most frequently studied. Based on a phylogenetic generalized least squares analysis of a data set on the reproductively homogenous clade of marsupials, we provide the first quantitative comparison of two hypotheses based on energetic constraints (maternal investment and seasonality) with two hypotheses that posit behavioral selection on relative brain size (social complexity and environmental interactions). We show that the two behavioral hypotheses have far less support than the constraint hypotheses. The only unambiguous associates of brain size are the constraint variables of litter size and seasonality. We also found no association between brain size and specific behavioral complexity categories within kangaroos, dasyurids, and possums. The largest-brained marsupials after phylogenetic correction are from low-seasonality New Guinea, supporting the notion that low seasonality represents greater nutrition safety for brain maintenance. Alternatively, low seasonality might improve the maternal support of offspring brain growth. The lack of behavioral brain size associates, found here and elsewhere, supports the general 'cognitive buffer hypothesis' as the best explanatory framework of mammalian brain size evolution. However, it is possible that brain size alone simply does not provide sufficient resolution on the question of how brain morphology and cognitive capacities coevolve.

Dispersal capacity predicts both population genetic structure and species richness in reef fishes.

Dispersal is a fundamental species characteristic that should directly affect both rates of gene flow among spatially distributed populations and opportunities for speciation. Yet no single trait associated with dispersal has been demonstrated to affect both micro- and macroevolutionary patterns of diversity across a diverse biological assemblage. Here, we examine patterns of genetic differentiation and species richness in reef fishes, an assemblage of over 7,000 species comprising approximately one-third of the extant bony fishes and over one-tenth of living vertebrates. In reef fishes, dispersal occurs primarily during a planktonic larval stage. There are two major reproductive and parental investment syndromes among reef fishes, and the differences between them have implications for dispersal: (1) benthic guarding fishes lay negatively buoyant eggs, typically guarded by the male parent, and from these eggs hatch large, strongly swimming larvae; in contrast, (2) pelagic spawning fishes release small floating eggs directly into the water column, which drift unprotected before small weakly swimming larvae hatch. Using phylogenetic comparative methods, we show that benthic guarders have significantly greater population structure than pelagic spawners and additionally that taxonomic families of benthic guarders are more species rich than families of pelagic spawners. Our findings provide a compelling case for the continuity between micro- and macroevolutionary processes of biological diversification and underscore the importance of dispersal-related traits in influencing the mode and tempo of evolution.

Phylogenetic correlates of extinction risk in mammals: species in older lineages are not at greater risk.

Phylogenetic information is becoming a recognized basis for evaluating conservation priorities, but associations between extinction risk and properties of a phylogeny such as diversification rates and phylogenetic lineage ages remain unclear. Limited taxon-specific analyses suggest that species in older lineages are at greater risk. We calculate quantitative properties of the mammalian phylogeny and model extinction risk as an ordinal index based on International Union for Conservation of Nature Red List categories. We test for associations between lineage age, clade size, evolutionary distinctiveness and extinction risk for 3308 species of terrestrial mammals. We show no significant global or regional associations, and three significant relationships within taxonomic groups. Extinction risk increases for evolutionarily distinctive primates and decreases with lineage age when lemurs are excluded. Lagomorph species (rabbits, hares and pikas) that have more close relatives are less threatened. We examine the relationship between net diversification rates and extinction risk for 173 genera and find no pattern. We conclude that despite being under-represented in the frequency distribution of lineage ages, species in older, slower evolving and distinct lineages are not more threatened or extinction-prone. Their extinction, however, would represent a disproportionate loss of unique evolutionary history.

Independent contrasts and PGLS regression estimators are equivalent.

We prove that the slope parameter of the ordinary least squares regression of phylogenetically independent contrasts (PICs) conducted through the origin is identical to the slope parameter of the method of generalized least squares (GLSs) regression under a Brownian motion model of evolution. This equivalence has several implications: 1. Understanding the structure of the linear model for GLS regression provides insight into when and why phylogeny is important in comparative studies. 2. The limitations of the PIC regression analysis are the same as the limitations of the GLS model. In particular, phylogenetic covariance applies only to the response variable in the regression and the explanatory variable should be regarded as fixed. Calculation of PICs for explanatory variables should be treated as a mathematical idiosyncrasy of the PIC regression algorithm. 3. Since the GLS estimator is the best linear unbiased estimator (BLUE), the slope parameter estimated using PICs is also BLUE. 4. If the slope is estimated using different branch lengths for the explanatory and response variables in the PIC algorithm, the estimator is no longer the BLUE, so this is not recommended. Finally, we discuss whether or not and how to accommodate phylogenetic covariance in regression analyses, particularly in relation to the problem of phylogenetic uncertainty. This discussion is from both frequentist and Bayesian perspectives.

Detrimental influence on performance of high temperature incubation in a tropical reptile: is cooler better in the tropics?

Global temperatures have risen over the last century, and are forecast to continue rising. Ectotherms may be particularly sensitive to changes in thermal regimes, and tropical ectotherms are more likely than temperate species to be influenced by changes in environmental temperature, because they may have evolved narrow thermal tolerances. Keelback snakes (Tropidonophis mairii) are tropical, oviparous reptiles. To quantify the effects of temperature on the morphology and physiology of hatchling keelbacks, clutches laid by wild-caught females were split and incubated at three temperatures, reflecting the average minimum, overall average and average maximum temperatures recorded at our study site. Upon hatching, the performance of neonates was examined at all three incubation temperatures in a randomized order over consecutive days. Hatchlings from the 'hot' treatment had slower burst swim speeds and swam fewer laps than hatchlings from the cooler incubation temperatures in all three test temperatures, indicating a low thermal optimum for incubation of this tropical species. There were no significant interactions between test temperature and incubation temperature across performance variables, suggesting phenotypic differences caused by incubation temperature did not acclimate this species to post-hatching conditions. Thus, keelback embryos appear evolutionarily adapted to development at cooler temperatures (relative to what is available in their habitat). The considerable reduction in hatchling viability and performance associated with a 3.5 °C increase in incubation temperature, suggests climate change may have significant population-level effects on this species. However, the offspring of three mothers exposed to the hottest incubation temperature were apparently resilient to high temperature, suggesting that this species may respond to selection imposed by thermal regime.

Bayesian models for comparative analysis integrating phylogenetic uncertainty.

BACKGROUND: Uncertainty in comparative analyses can come from at least two sources: a) phylogenetic uncertainty in the tree topology or branch lengths, and b) uncertainty due to intraspecific variation in trait values, either due to measurement error or natural individual variation. Most phylogenetic comparative methods do not account for such uncertainties. Not accounting for these sources of uncertainty leads to false perceptions of precision (confidence intervals will be too narrow) and inflated significance in hypothesis testing (e.g. p-values will be too small). Although there is some application-specific software for fitting Bayesian models accounting for phylogenetic error, more general and flexible software is desirable. METHODS: We developed models to directly incorporate phylogenetic uncertainty into a range of analyses that biologists commonly perform, using a Bayesian framework and Markov Chain Monte Carlo analyses. RESULTS: We demonstrate applications in linear regression, quantification of phylogenetic signal, and measurement error models. Phylogenetic uncertainty was incorporated by applying a prior distribution for the phylogeny, where this distribution consisted of the posterior tree sets from Bayesian phylogenetic tree estimation programs. The models were analysed using simulated data sets, and applied to a real data set on plant traits, from rainforest plant species in Northern Australia. Analyses were performed using the free and open source software OpenBUGS and JAGS. CONCLUSIONS: Incorporating phylogenetic uncertainty through an empirical prior distribution of trees leads to more precise estimation of regression model parameters than using a single consensus tree and enables a more realistic estimation of confidence intervals. In addition, models incorporating measurement errors and/or individual variation, in one or both variables, are easily formulated in the Bayesian framework. We show that BUGS is a useful, flexible general purpose tool for phylogenetic comparative analyses, particularly for modelling in the face of phylogenetic uncertainty and accounting for measurement error or individual variation in explanatory variables. Code for all models is provided in the BUGS model description language.

Inferring extinction of mammals from sighting records, threats, and biological traits.

For species with five or more sightings, quantitative techniques exist to test whether a species is extinct on the basis of distribution of sightings. However, 70% of purportedly extinct mammals are known from fewer than five sightings, and such models do not include some important indicators of the likelihood of extinction such as threats, biological traits, search effort, and demography. Previously, we developed a quantitative method that we based on species' traits in which we used Cox proportional hazards regression to calculate the probability of rediscovery of species regarded as extinct. Here, we used two versions of the Cox regression model to determine the probability of extinction in purportedly extinct mammals and compared the results of these two models with those of stationary Poisson, nonparametric, and Weibull sighting-distribution models. For mammals with five or more sightings, the stationary Poisson model categorized all but two critically endangered (flagged as possibly extinct) species in our data set as extinct, and results with this model were consistent with current categories of the International Union for the Conservation of Nature. The scores of probability of rediscovery for individual species in one version of our Cox regression model were correlated with scores assigned by the stationary Poisson model. Thus, we used this Cox regression model to determine the probability of extinction of mammals with sparse records. On the basis of the Cox regression model, the most likely mammals to be rediscovered were the Montane monkey-faced bat (Pteralopex pulchra), Armenian myotis (Myotis hajastanicus), Alcorn's pocket gopher (Pappogeomys alcorni), and Wimmer's shrew (Crocidura wimmeri). The Cox model categorized two species that have recently disappeared as extinct: the baiji (Lipotes vexillifer) and the Christmas Island pipistrelle (Pipistrellus murrayi). Our new method can be used to test whether species with few records or recent last-sighting dates are likely to be extinct.

Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild.

Females often mate with several males before producing offspring. Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival. This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring. Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring. Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring. Surprisingly, however, there is no unequivocal evidence for this process. Here, by experimentally assigning mates to females, we show that polyandry greatly increases offspring survival in the Australian marsupial Antechinus stuartii. DNA profiling shows that males that gain high paternity under sperm competition sire offspring that are more viable. This beneficial effect occurs in both the laboratory and the wild. Crucially, there are no confounding non-genetic maternal effects that could arise if polyandry increases female investment in a particular reproductive event because A. stuartii is effectively semelparous. Our results therefore show that polyandry improves female lifetime fitness in nature. The threefold increase in offspring survival is not negated by a decline in maternal lifespan and is too large to be offset by an equivalent decline in the reproductive performance of surviving offspring.

Correlates of rediscovery and the detectability of extinction in mammals.

Extinction is difficult to detect, even in well-known taxa such as mammals. Species with long gaps in their sighting records, which might be considered possibly extinct, are often rediscovered. We used data on rediscovery rates of missing mammals to test whether extinction from different causes is equally detectable and to find which traits affect the probability of rediscovery. We find that species affected by habitat loss were much more likely to be misclassified as extinct or to remain missing than those affected by introduced predators and diseases, or overkill, unless they had very restricted distributions. We conclude that extinctions owing to habitat loss are most difficult to detect; hence, impacts of habitat loss on extinction have probably been overestimated, especially relative to introduced species. It is most likely that the highest rates of rediscovery will come from searching for species that have gone missing during the 20th century and have relatively large ranges threatened by habitat loss, rather than from additional effort focused on charismatic missing species.

Picante: R tools for integrating phylogenies and ecology.

SUMMARY: Picante is a software package that provides a comprehensive set of tools for analyzing the phylogenetic and trait diversity of ecological communities. The package calculates phylogenetic diversity metrics, performs trait comparative analyses, manipulates phenotypic and phylogenetic data, and performs tests for phylogenetic signal in trait distributions, community structure and species interactions. AVAILABILITY: Picante is a package for the R statistical language and environment written in R and C, released under a GPL v2 open-source license, and freely available on the web (http://picante.r-forge.r-project.org) and from CRAN (http://cran.r-project.org).

Causes and consequences of variation in plant population growth rate: a synthesis of matrix population models in a phylogenetic context.

Explaining variation in population growth rates is fundamental to predicting population dynamics and population responses to environmental change. In this study, we used matrix population models, which link birth, growth and survival to population growth rate, to examine how and why population growth rates vary within and among 50 terrestrial plant species. Population growth rates were more similar within species than among species; with phylogeny having a minimal influence on among-species variation. Most population growth rates decreased over the observation period and were negatively autocorrelated between years; that is, higher than average population growth rates tended to be followed by lower than average population growth rates. Population growth rates varied more through time than space; this temporal variation was due mostly to variation in post-seedling survival and for a subset of species was partly explained by response to environmental factors, such as fire and herbivory. Stochastic population growth rates departed from mean matrix population growth rate for temporally autocorrelated environments. Our findings indicate that demographic data and models of closely related plant species cannot necessarily be used to make recommendations for conservation or control, and that post-seedling survival and the sequence of environmental conditions are critical for determining plant population growth rate.

Nitrogen and phosphorus additions negatively affect tree species diversity in tropical forest regrowth trajectories.

Nutrient enrichment is increasingly affecting many tropical ecosystems, but there is no information on how this affects tree biodiversity. To examine dynamics in vegetation structure and tree species biomass and diversity, we annually remeasured tree species before and for six years after repeated additions of nitrogen (N) and phosphorus (P) in permanent plots of abandoned pasture in Amazonia. Nitrogen and, to a lesser extent, phosphorus addition shifted growth among woody species. Nitrogen stimulated growth of two common pioneer tree species and one common tree species adaptable to both high- and low-light environments, while P stimulated growth only of the dominant pioneer tree Rollinia exsucca (Annonaceae). Overall, N or P addition reduced tree assemblage evenness and delayed tree species accrual over time, likely due to competitive monopolization of other resources by the few tree species responding to nutrient enrichment with enhanced establishment and/or growth rates. Absolute tree growth rates were elevated for two years after nutrient addition. However, nutrient-induced shifts in relative tree species growth and reduced assemblage evenness persisted for more than three years after nutrient addition, favoring two nutrient-responsive pioneers and one early-secondary tree species. Surprisingly, N + P effects on tree biomass and species diversity were consistently weaker than N-only and P-only effects, because grass biomass increased dramatically in response to N + P addition. The resulting intensified competition probably prevented an expected positive N + P synergy in the tree assemblage. Thus, N or P enrichment may favor unknown tree functional response types, reduce the diversity of coexisting species, and delay species accrual during structurally and functionally complex tropical rainforest secondary succession.

Strategic (adaptive) hypothermia in bull dromedary camels during rut; could it increase reproductive success?

In this study of body temperatures (T(b)) in free ranging dromedary camels, we found that bulls in rut start the days cooler. Daily minima during rut averaged 0.6 degrees C lower than at other times (95% CI 0.27-0.94 degrees C) and daily maxima averaged 0.45 degrees C higher (95% CI -0.01 to -0.91 degrees C), increasing the daily T(b) cycle. Knut Schmidt-Nielsen described a similar pattern in captive dromedaries deprived of water in hot conditions, which he interpreted as a strategy to conserve water. Our observations were made in winter and with water freely available. Dromedaries can apparently employ heterothermy for more than just water conservation. In the strenuous daily contests between rival bulls in rut, a lower T(b) early in the day should extend the time for which a contestant can challenge or defend before heat stress becomes a problem. Calculations show that lowering T(b) by even 0.6 degrees C extends that time by more than 30 min, and many daily minima during rut were lower than that. Because the eventual winner of contests gains or retains a herd of females, we speculate that cooler T(b) at the start of daily contests confers an advantage which translates directly into increased reproductive success.

Manganese accumulates in the brain of northern quolls (Dasyurus hallucatus) living near an active mine.

Mining is fundamental to the Australian economy, yet little is known about how potential contaminants bioaccumulate and affect wildlife living near active mining sites. Here, we show using air sampling that fine manganese dust within the respirable size range is found at levels exceeding international recommendations even 20 km from manganese extraction, processing, and storage facilities on Groote Eylandt, Northern Territory. Endangered northern quolls (Dasyurus hallucatus) living near mining sites were found to have elevated manganese concentrations within their hair, testes, and in two brain regions-the neocortex and cerebellum, which are responsible for sensory perception and motor function, respectively. Accumulation in these organs has been associated with adverse reproductive and neurological effects in other species and could affect the long-term population viability of northern quolls.

Accumulation and partitioning of heavy metals in mangroves: a synthesis of field-based studies.

We report the findings of a comparative analysis examining patterns of accumulation and partitioning of the heavy metals copper (Cu), lead (Pb) and zinc (Zn) in mangroves from available field-based studies to date, employing both species level analyses and a phylogenetic approach. Despite mangroves being a taxonomically diverse group, metal accumulation and partitioning for all metals examined were broadly similar across genera and families. Patterns of metal accumulation were also similar regardless of whether species were classified as salt secreting or non-secreting. Metals were accumulated in roots to concentrations similar to those of adjacent sediments with root bio-concentration factors (BCF; ratio of root metal to sediment metal concentration) of 1< or =. Root BCFs were constant across the exposure range for all metals. Metal concentrations in leaves were half that of roots or lower. Essential metals (Cu and Zn; translocation factors (TF; ratio of leaf metal to root metal concentration) of 0.52 and 0.53, and leaf BCFs of 0.47 and 0.51, respectively) showed greater mobility than non-essential metals (Pb; TF of 0.31 and leaf BCF of 0.11). Leaf BCFs for the essential metals Cu and Zn decreased as environmental concentrations increased. The non-essential metal Pb was excluded from leaf tissue regardless of environmental concentrations. Thus mangroves as a group tend to operate as excluder species for non-essential metals and regulators of essential metals. For phytoremediation initiatives, mangrove ecosystems are perhaps best employed as phytostabilisers, potentially aiding in the retention of toxic metals and thereby reducing transport to adjacent estuarine and marine systems.

Mule deer spatial association patterns and potential implications for transmission of an epizootic disease.

Animal social behaviour can have important effects on the long-term dynamics of diseases. In particular, preferential spatial relationships between individuals can lead to differences in the rates of disease spread within a population. We examined the concurrent influence of genetic relatedness, sex, age, home range overlap, time of year, and prion disease status on proximal associations of adult Rocky Mountain mule deer (Odocoileus hemionus hemionus) in a chronic wasting disease endemic area. We also quantified the temporal stability of these associations across different sex, age, and disease status classes. We used three years of high frequency telemetry data from 74 individuals to record encounters within 25 m of each other, and to calculate seasonal home range overlap measured by volume of intersection (VI). The strength of pairwise spatial association between adult mule deer was independent of genetic relatedness, age and disease status. Seasonal variation in association strength was not consistent across years, perhaps due to annual changes in weather conditions. The influence of home range overlap on association strength varied seasonally, whereby associations were stronger in pre-rut and fawning than in the rest of the seasons. The sexes of individuals also interacted with both VI and season. At increasing levels of VI, associations were stronger between females than between males and between females and males. The strongest associations in pre-rut were between males, while the strongest in rut were between females and males. The temporal stability of associations was markedly dependant on the sex and the diagnosis of the associating pair. Our findings highlight the importance of considering concurrent effects of biological and environmental factors when seeking to understand the role of social preference in behavioural ecology and disease spread. Applying this knowledge in epidemiological modelling will shed light on the dynamics of disease transmission among mule deer.