Research Article: Ecology Drives the Worldwide Distribution of Human Diseases

Date Published: June 15, 2004

Publisher: Public Library of Science

Author(s): Vanina Guernier, Michael E Hochberg, Jean-François Guégan

Abstract: Identifying the factors underlying the origin and maintenance of the latitudinal diversity gradient is a central problem in ecology, but no consensus has emerged on which processes might generate this broad pattern. Interestingly, the vast majority of studies exploring the gradient have focused on free-living organisms, ignoring parasitic and infectious disease (PID) species. Here, we address the influence of environmental factors on the biological diversity of human pathogens and their global spatial organization. Using generalized linear multivariate models and Monte Carlo simulations, we conducted a series of comparative analyses to test the hypothesis that human PIDs exhibit the same global patterns of distribution as other taxonomic groups. We found a significant negative relationship between latitude and PID species richness, and a nested spatial organization, i.e., the accumulation of PID species with latitude, over large spatial scales. Additionally, our results show that climatic factors are of primary importance in explaining the link between latitude and the spatial pattern of human pathogens. Based on our findings, we propose that the global latitudinal species diversity gradient might be generated in large part by biotic interactions, providing strong support for the idea that current estimates of species diversity are substantially underestimated. When parasites and pathogens are included, estimates of total species diversity may increase by more than an order of magnitude.

Partial Text: Generally, the number of plant and animal species declines as one moves away from the equator (Pianka 1966; Stevens 1989, 1992; Rohde 1992; Brown 1995; Kaufman 1995; Rosenzweig 1995; Roy et al. 1998; Huston 1999; Chown and Gaston 2000; Hawkins and Porter 2001). This pattern, known as the latitudinal species diversity gradient, has been documented for many contemporary taxonomic groups (see Brown 1995; Rosenzweig 1995; Gaston and Blackburn 2000; Allen et al. 2002; Stevens et al. 2003). Over 30 hypotheses have been proposed to explain it (Rohde 1992), and it is only over the past several years that the most credible candidates have been identified; these are hypotheses related to area, energy, and time (Gaston and Blackburn 2000; Rahbek and Graves 2001) and to habitat heterogeneity and geometric constraints (Rahbek and Graves 2001).

To our knowledge, this is the most comprehensive report of how PID species richness varies with latitude and the ecological factors behind observed trends. Our results support previous studies in showing that species diversity increases as one proceeds from the poles to the equator (Pianka 1966; Stevens 1989; Rohde 1992; Brown 1995; Rosenzweig 1995; Chown and Gaston 2000). This similarity in the patterns of PID species and free-living organisms suggests that common mechanisms are at work. Regardless of whether PID richness simply tracks host diversity or, rather, is determined to a greater extent by exogenous factors, our analyses indicate that the most likely explanation for these patterns is the climatically-based energy hypothesis, i.e., that energy availability generates and maintains species richness gradients (Rohde 1992; Gaston and Blackburn 2000; Allen et al. 2002; Hawkins et al. 2003). Many studies have identified correlations between gradients in species diversity and variation in climate (Hill et al. 1999). Climate, in turn, largely determines the species of plants and animals that live in those areas. According to our results—and in contrast to the results of Allen and colleagues (2002), who showed that environmental temperature was the best predictor of species diversity for terrestrial, freshwater, and marine ectotherm taxa—the maximum range of precipitation is highly correlated with the latitudinal gradient of pathogen species, with diversity significantly increasing with this climate-based factor. Interestingly, the annual variation of precipitation around the mean (and not the mean itself) was the best predictor overall of pathogen species distribution. This suggests that pathogen species, their vectors, or their hosts tend to be adapted to regions having more contrasted wetness and dryness conditions through the year (i.e., in tropical regions). Many parasites obviously require water or humid conditions to complete their life cycle, e.g., vector-borne diseases. So, the physical factor of precipitation variation may affect parasitic and infectious microorganism diversity, if the biological cyclicity of a variety of parasitic and infectious stages have adapted to the variability of precipitation. This might be why “latitude” does not appear in the minimal generalized linear models (GLIMs) for explaining the richnesses of bacteria, directly transmitted viruses, and fungi, these taxa being “internal” to the host, so less directly affected by environmental variability. Moreover, these taxa may more readily spread over longer distances via their hosts, and this should minimize the impact of environmental conditions. In contrast, taxa with “external” stages, like helminths or vector-transmitted pathogens, are more influenced by their environment. Nevertheless, other causes might explain why certain taxa do not conform to the general pattern, notably (1) the absence of possible explanatory variables in the GLIMs, (2) missing or imprecise information due to the large scale of our study, or (3) the real absence of correlations between the spatial distributions of certain taxonomic groups and the variables considered here.



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