John L. Gittleman

Global trends in emerging infectious diseases.

Emerging infectious diseases (EIDs) are a significant burden on global economies and public health. Their emergence is thought to be driven largely by socio-economic, environmental and ecological factors, but no comparative study has explicitly analysed these linkages to understand global temporal and spatial patterns of EIDs. Here we analyse a database of 335 EID ‘events’ (origins of EIDs) between 1940 and 2004, and demonstrate non-random global patterns. EID events have risen significantly over time after controlling for reporting bias, with their peak incidence (in the 1980s) concomitant with the HIV pandemic. EID events are dominated by zoonoses (60.3% of EIDs): the majority of these (71.8%) originate in wildlife (for example, severe acute respiratory virus, Ebola virus), and are increasing significantly over time. We find that 54.3% of EID events are caused by bacteria or rickettsia, reflecting a large number of drug-resistant microbes in our database. Our results confirm that EID origins are significantly correlated with socio-economic, environmental and ecological factors, and provide a basis for identifying regions where new EIDs are most likely to originate (emerging disease ‘hotspots’). They also reveal a substantial risk of wildlife zoonotic and vector-borne EIDs originating at lower latitudes where reporting effort is low. We conclude that global resources to counter disease emergence are poorly allocated, with the majority of the scientific and surveillance effort focused on countries from where the next important EID is least likely to originate.

The delayed rise of present-day mammals

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic ‘fuses’ leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today’s mammals.

Predicting extinction risk in declining species

What biological attributes predispose species to the risk of extinction? There are many hypotheses but so far there has been no systematic analysis for discriminating between them. Using complete phylogenies of contemporary carnivores and primates, we present, to our knowledge, the first comparative test showing that high trophic level, low population density, slow life history and, in particular, small geographical range size are all significantly and independently associated with a high extinction risk in declining species. These traits together explain nearly 50% of the total between–species variation in extinction risk. Much of the remaining variation can be accounted for by external anthropogenic factors that affect species irrespective of their biology.

The biodiversity of species and their rates of extinction, distribution, and protection

Background A principal function of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) is to “perform regular and timely assessments of knowledge on biodiversity.” In December 2013, its second plenary session approved a program to begin a global assessment in 2015. The Convention on Biological Diversity (CBD) and five other biodiversity-related conventions have adopted IPBES as their science-policy interface, so these assessments will be important in evaluating progress toward the CBD’s Aichi Targets of the Strategic Plan for Biodiversity 2011–2020. As a contribution toward such assessment, we review the biodiversity of eukaryote species and their extinction rates, distributions, and protection. We document what we know, how it likely differs from what we do not, and how these differences affect biodiversity statistics. Interestingly, several targets explicitly mention “known species”—a strong, if implicit, statement of incomplete knowledge. We start by asking how many species are known and how many remain undescribed. We then consider by how much human actions inflate extinction rates. Much depends on where species are, because different biomes contain different numbers of species of different susceptibilities. Biomes also suffer different levels of damage and have unequal levels of protection. How extinction rates will change depends on how and where threats expand and whether greater protection counters them. Different visualizations of species biodiversity. (A) The distributions of 9927 bird species. (B) The 4964 species with smaller than the median geographical range size

PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals

Analyses of life-history, ecological, and geographic trait differences among species, their causes, correlates, and likely consequences are increasingly important for understanding and conserving biodiversity in the face of rapid global change. Assembling multispecies trait data from diverse literature sources into a single comprehensive data set requires detailed consideration of methods to reliably compile data for particular species, and to derive single estimates from multiple sources based on different techniques and definitions. Here we describe PanTHERIA, a species-level data set compiled for analysis of life history, ecology, and geography of all known extant and recently extinct mammals. PanTHERIA is derived from a database capable of holding multiple geo-referenced values for variables within a species containing 100 740 lines of biological data for extant and recently extinct mammalian species, collected over a period of three years by 20 individuals. PanTHERIA also includes spatial databases o...

Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia)

One way to build larger, more comprehensive phylogenies is to combine the vast amount of phylogenetic information already available. We review the two main strategies for accomplishing this (combining raw data versus combining trees), but employ a relatively new variant of the latter: supertree construction. The utility of one supertree technique, matrix representation using parsimony analysis (MRP), is demonstrated by deriving a complete phylogeny for all 271 extant species of the Garnivora from 177 literature sources. Beyond providing a ‘consensus’ estimate of carnivore phylogeny, the tree also indicates taxa for which the relationships remain controversial (e.g. the red panda; within canids, felids, and hyaenids) or have not been studied in any great detail (e.g. herpestids, viverrids, and intrageneric relationships in the procyonids). Times of divergence throughout the tree were also estimated from 74 literature sources based on both fossil and molecular data. We use the phylogeny to show that some lineages within the Mustelinae and Canidae contain significantly more species than expected for their age, illustrating the trees utility for studies of macroevolution. It will also provide a useful foundation for comparative and conservational studies involving the carnivores.

Early bursts of body size and shape evolution are rare in comparative data.

George Gaylord Simpson famously postulated that much of lifes diversity originated as adaptive radiations—more or less simultaneous divergences of numerous lines from a single ancestral adaptive type. However, identifying adaptive radiations has proven difficult due to a lack of broad‐scale comparative datasets. Here, we use phylogenetic comparative data on body size and shape in a diversity of animal clades to test a key model of adaptive radiation, in which initially rapid morphological evolution is followed by relative stasis. We compared the fit of this model to both single selective peak and random walk models. We found little support for the early‐burst model of adaptive radiation, whereas both other models, particularly that of selective peaks, were commonly supported. In addition, we found that the net rate of morphological evolution varied inversely with clade age. The youngest clades appear to evolve most rapidly because long‐term change typically does not attain the amount of divergence predicted from rates measured over short time scales. Across our entire analysis, the dominant pattern was one of constraints shaping evolution continually through time rather than rapid evolution followed by stasis. We suggest that the classical model of adaptive radiation, where morphological evolution is initially rapid and slows through time, may be rare in comparative data.

Global distribution and conservation of rare and threatened vertebrates

Global conservation strategies commonly assume that different taxonomic groups show congruent geographical patterns of diversity, and that the distribution of extinction-prone species in one group can therefore act as a surrogate for vulnerable species in other groups when conservation decisions are being made. The validity of these assumptions remains unclear, however, because previous tests have been limited in both geographical and taxonomic extent. Here we use a database on the global distribution of 19,349 living bird, mammal and amphibian species to show that, although the distribution of overall species richness is very similar among these groups, congruence in the distribution of rare and threatened species is markedly lower. Congruence is especially low among the very rarest species. Cross-taxon congruence is also highly scale dependent, being particularly low at the finer spatial resolutions relevant to real protected areas. ‘Hotspots’ of rarity and threat are therefore largely non-overlapping across groups, as are areas chosen to maximize species complementarity. Overall, our results indicate that ‘silver-bullet’ conservation strategies alone will not deliver efficient conservation solutions. Instead, priority areas for biodiversity conservation must be based on high-resolution data from multiple taxa.

Adaptation: Statistics and a Null Model for Estimating Phylogenetic Effects

-Tests of adaptive explanations are often critically confounded by phylogenetic heritage. In this paper we propose statistics and a null model for estimating phylogenetic effects in comparative data. We apply a model-independent measure of autocorrelation (Morans I) for estimating whether cross-taxonomic trait variation is related to phylogeny. We develop a phylogenetic correlogram for assessing how autocorrelation varies with patristic distance and for judging the appropriateness and effectiveness of an autoregressive model. We then revise Cheverud et al.s (1985, Evolution, 39:1335-1351) autocorrelational model to incorporate greater flexibility in the relation between trait variation and phylogenetic distance. Finally, we analyze various comparative data sets (body weight in carnivores, clutch size in birds) and phylogenies (morphological, molecular) to illustrate some of the complications that may arise from using an autoregressive model and to explore the effects of different weighting matrices in adjusting for these complications. Although our approach has limitations, it is both effective in partitioning trait variation into adaptive and phylogenetic components and flexible in adjusting to peculiarities in taxonomic distribution. [Phylogenetic effects; phylogenetic correlation; autoregressive models; comparative methods.] The comparative method is commonly used to investigate adaptation. A researcher examines the attributes of a number of species. Statistical analyses of these data are then used to formulate and test adaptive hypotheses of life history, morphology, physiology, demography, and behavior (e.g., Clutton-Brock and Harvey, 1977; Damuth, 1981; Gittleman and Harvey, 1982; Harvey and Clutton-Brock, 1985; Gittleman, 1986a, b; Huey and Bennett, 1987). If traits are analyzed across a broad range of independently derived taxa, the resulting adaptive explanations may be quite robust (Clutton-Brock and Harvey, 1984; Huey and Bennett, 1986; Gittleman, 1989). If, however, the data reflect a highly structured phylogeny (with little statistical independence), results may be misleading (Felsenstein, 1985). To neglect phylogeny is to invite type I and type II errors (see Fig. 1). A number of techniques have been developed for removing the effects of phylogeny (see reviews in Huey, 1987; Pagel and Harvey, 1988; Gittleman, 1989; Burghardt and Gittleman, 1990). Some of these techniques are better suited for particular variables or certain evolutionary questions, and all possess limitations. Nominal or categorical data (e.g., mating system: monogamy, polygamy) may be analyzed by evaluating the agreement between the variation in a trait and an accepted phylogeny (Dobson, 1985; Greene, 1986) or by using outgroup comparisons to identify evolutionary transitions among traits (Gittleman, 1981; Ridley, 1983). For quantitative data, there are several strategies. One may avoid spurious correlation by averaging over closely related species, thereby reducing the degrees of freedom and significance of the correlation. Alternatively, one may transform the data so that phylogenetically disparate groups appear on a common scale. Even within this general framework there are several methods for evaluating the association between the ordinal or continuous values of a trait and phylogeny: (1) Nested analysis of variance partitions the total variation in a continuous character among various taxonomic levels. By selecting the taxonomic level that accounts for the greatest proportion of the total variance as the appropriate level for analysis, this method attempts to control for bias from low-level clades that are both uniform and speciesrich (Harvey and Mace, 1982; Harvey and

THE IMPACT OF SPECIES CONCEPT ON BIODIVERSITY STUDIES

Species are defined using a variety of different operational techniques. While discussion of the various methodologies has previously been restricted mostly to taxonomists, the demarcation of species is also crucial for conservation biology. Unfortunately, different methods of diagnosing species can arrive at different entities. Most prominently, it is widely thought that use of a phylogenetic species concept may lead to recognition of a far greater number of much less inclusive units. As a result, studies of the same group of organisms can produce not only different species identities but also different species range and number of individuals. To assess the impact of different definitions on conservation issues, we collected instances from the literature where a group of organisms was categorized both under phylogenetic and nonphylogenetic concepts. Our results show a marked difference, with surveys based on a phylogenetic species concept showing more species (48%) and an associated decrease in population size and range. We discuss the serious consequences of this trend for conservation, including an apparent change in the number of endangered species, potential political fallout, and the difficulty of deciding what should be conserved.