Functional trait space and the latitudinal diversity gradient

The processes causing the latitudinal gradient in species richness remain elusive. Ecological theories for the origin of biodiversity gradients, such as competitive exclusion, neutral dynamics, and environmental filtering, make predictions for how functional diversity should vary at the alpha (within local assemblages), beta (among assemblages), and gamma (regional pool) scales. We test these predictions by quantifying hypervolumes constructed from functional traits representing major axes of plant strategy variation (specific leaf area, plant height, and seed mass) in tree assemblages spanning the temperate and tropical New World. Alpha-scale trait volume decreases with absolute latitude and is often lower than sampling expectation, consistent with environmental filtering theory. Beta-scale overlap decays with geographic distance fastest in the temperate zone, again consistent with environmental filtering theory. In contrast, gamma-scale trait space shows a hump-shaped relationship with absolute latitude, consistent with no theory. Furthermore, the overall temperate trait hypervolume was larger than the overall tropical hypervolume, indicating that the temperate zone permits a wider range of trait combinations or that niche packing is stronger in the tropical zone. Although there are limitations in the data, our analyses suggest that multiple processes have shaped trait diversity in trees, reflecting no consistent support for any one theory.Species richness increases toward the equator (1, 2) in major clades of both extant and extinct species of plants and animals (3, 4). The generality of the pattern hints at a correspondingly general explanation, yet the latitudinal gradient in species richness remains one of ecology’s greatest unsolved puzzles. Long-running debates over the causes of the latitudinal gradient of species richness have focused on ecological, evolutionary, and geographic explanations (5–10). Although there has been some progress (11), it is also increasingly clear that there are numerous obstacles to understanding the primary drivers of the latitudinal gradient, including an ever-increasing number of hypotheses (12, 13), challenges in clearly separating their interdependencies (14, 15), and difficulties in rigorously falsifying their assumptions and predictions (16).More powerful tests of biodiversity theories need to move beyond species richness and instead explicitly focus on the mechanisms generating the gradient, by recasting the theories in terms of other measures of diversity, such as functional diversity (17–19). For example, explanations that assume species richness is limited by resource availability have often focused on the strength of species interactions, life history differences, and environmental constraints on how species pack into niche space (20). Evolutionary hypotheses have focused on differences in diversification rates, as well as the influence of species interactions on diversification rates (9). These interaction-based explanations implicitly refer to the degree of ecological differentiation among species, and therefore to trait dispersion within clades and assemblages, suggesting that patterns of functional diversity may provide a more powerful test of theory than taxonomic richness (21).A particularly important concept that unifies many ecological and evolutionary theories is the concept of the Hutchinsonian multidimensional niche (22). Hutchinsonian niches can be quantified by assessing the functional trait hypervolumes that characterize phenotypic space occupied by a set of species. Quantifying the volume, overlap, and packing of functional trait space at different spatial scales enables inferences about how differing ecological and evolutionary processes structure functional diversity and ecological strategies (23, 24).Here, we recast several contrasting hypotheses for the latitudinal gradient in terms of functional trait space. We focus on the proximate ecological mechanisms that ultimately can influence evolutionary processes. We quantify tree functional trait space across latitude at three spatial scales: (i) within assemblages (alpha), (ii) among assemblages (beta), and (iii) among biomes (gamma). For alpha and beta analyses, we use tree species assemblage data from 620 standardized 0.1-ha forest plots (Fig. 1A); for gamma analyses, we calculated the latitudinal range distributions for 520 New World tree species where we had sufficient data on geographic distribution and functional traits. In total, across all analyses, we used paired geographic occurrence data with trait data for 6,839 tree species.Open in a separate windowFig. 1.(A) Spatial distribution of the 620 0.1-ha forest plots used in this study. Plots are colored by richness. Plots cover most of the New World forested climate space (Fig. S1). (B) Relationship between absolute latitude and alpha hypervolume for tropical (red triangles) and temperate (blue pluses) plots. (C) Alpha hypervolume as a function of effective species richness (number of species with full trait coverage). We compare this hypervolume with a null expectation based on sampling the same number of species from the regional pool (median, dark gray line; 90% quantile range, light gray envelope).We primarily measured hypervolumes for three central traits hypothesized to characterize major axes of ecological strategy variation (25): specific leaf area (SLA), maximum height, and seed mass. SLA represents the tradeoff between leaf longevity and maximum photosynthetic rate (26); height is important for light competition and dispersal (27); and seed mass represents tradeoffs between fecundity, dispersal, and seedling survival (27). Although whole-plant resource strategies can be more fully assessed in higher dimensions (28, 29), we focus on these traits because of data availability (Materials and Methods). We use a hypervolume algorithm for calculating the volume and overlap of trait space (30) (Materials and Methods). All hypervolumes are reported in units of SDs of centered and scaled log-transformed trait values, raised to the power of the number of trait dimensions used.At all scales, our overall results and conclusions are similar (i) with and without gap-filling missing data, (ii) if we use convex hulls instead of hypervolumes to calculate trait spaces, and (iii) if we include additional trait axes. Additional details are given in Figs. S2–S7.     

Chronic fatigue syndrome and personality: A case-control study using the alternative five factor model

Neuroticism is the personality dimension most frequently associated with chronic fatigue syndrome (CFS). Most studies have also shown that CFS patients are less extraverted than non-CFS patients, but results have been inconsistent, possibly because the facets of the extraversion dimension have not been separately analyzed. This study has the following aims: to assess the personality profile of adults with CFS using the Alternative Five-Factor Model (AFFM), which considers Activity and Sociability as two separate factors of Extraversion, and to test the discriminant validity of a measure of the AFFM, the Zuckerman–Kuhlman Personality Questionnaire, in differentiating CFS subjects from normal-range matched controls. The CFS sample consisted of 132 consecutive patients referred for persistent fatigue or pain to the Department of Medicine of a university hospital. These were compared with 132 matched normal population controls. Significantly lower levels of Activity and significantly higher levels of Neuroticism-Anxiety best discriminated CFS patients from controls. The results are consistent with existing data on the relationship between Neuroticism and CFS, and clarify the relationship between Extraversion and CFS by providing new data on the relationship of Activity to CFS.     

From the Cover: Strong upslope shifts in Chimborazo's vegetation over two centuries since Humboldt

Global climate change is driving species poleward and upward in high-latitude regions, but the extent to which the biodiverse tropics are similarly affected is poorly known due to a scarcity of historical records. In 1802, Alexander von Humboldt ascended the Chimborazo volcano in Ecuador. He recorded the distribution of plant species and vegetation zones along its slopes and in surrounding parts of the Andes. We revisited Chimborazo in 2012, precisely 210 y after Humboldt’s expedition. We documented upward shifts in the distribution of vegetation zones as well as increases in maximum elevation limits of individual plant taxa of >500 m on average. These range shifts are consistent with increased temperatures and glacier retreat on Chimborazo since Humboldt’s study. Our findings provide evidence that global warming is strongly reshaping tropical plant distributions, consistent with Humboldt’s proposal that climate is the primary control on the altitudinal distribution of vegetation.The biological impacts of ongoing climate change (1) are already apparent in species’ poleward and upslope range shifts and earlier spring events (2–9). However, most studies stem from high-latitude areas and are generally restricted to dynamics across the past few decades (10). To our knowledge, only three previous resurveys have studied range shifts of tropical plant taxa, all at <4,000 m in elevation (7, 8, 11). Modeling (12) and paleoecological studies (13) suggest that tropical montane vegetation should be highly sensitive to climate change. However, researchers strongly debate whether tropical plants are tracking warming temperatures along elevation gradients, with most (although scarce) studies indicating they are lagging behind (cf. 14, 15). Such lags could have negative effects on the distributions of species dependent on certain plant taxa, e.g., as a food source (16). The question is particularly urgent given the growing evidence of systematically stronger warming rates in high-mountain environments (17).The legacy and works of Alexander von Humboldt (1769–1859) not only constitute the foundation of biogeography, but also what is likely the oldest dataset on altitudinal ranges of plant species. The observations recorded by Humboldt and Aimé Bonpland (1773–1858) during their travels in Central and South America, and synthesized in a Tableau of Mt. Chimborazo (summit 6,268 m above sea level) and accompanying essay (18), provide a unique opportunity to study tropical vegetation changes over a period of 210 y. To our knowledge, this period is more than twice as long as any previous resurvey study based on historical biodiversity records (11, 19). We revisited the upper slopes of the Chimborazo volcano in June 2012. Our aim was to record the current elevational distribution of plants and test for upward shifts since Humboldt’s expedition, as a response to anthropogenic global warming. We sampled plant species presence and abundance along transects every 100 m of elevation between 3,800 and 5,200 m. Three main findings, comparing our surveys to Humboldt’s data, support strong upward shifts of plant distributions: a higher upper limit for plant growth, increased elevation of vegetation zones, and upward shifts in the upper range limits of most individual taxa.     

Is it just an obstructive pyelonephritis?

Pyelocaliceal obstruction is a diagnostic challenge, and it is important to identify the obstruction cause. Some patients present extra‐renal compressive masses that need further imagiologic investigation and a biopsy, to establish the diagnosis.     

Headache and multiple sclerosis: a population-based case-control study in Catania, Sicily

We carried out a population-based case-control study to evaluate the association between multiple sclerosis (MS) and headache. We had previously determined the incidence of MS during 1990-1999 in Catania, Sicily, identifying 155 incident MS patients; these subjects underwent a telephone interview using a standardized questionnaire for headache. Diagnosis and classification of headaches were made according to International Headache Society criteria (1988). A control group was selected from the general population through random digit dialling. One hundred and one (65.2%) MS patients, of the 155 identified, and 101 controls were screened for headaches. Fifty-eight (57.4%) MS patients and 38 (37.2%) controls fulfilled the diagnostic criteria of headache. A significant association between MS and headache was found with an adjusted odds ratio, estimated by logistic regression, of 2.18 (95% confidence interval 1.27, 3.93). Frequency of headaches in our MS population is higher than in the general population, supporting the hypothesis of a possible association between these two conditions.     

The adaptive challenge of extreme conditions shapes evolutionary diversity of plant assemblages at continental scales

The tropical conservatism hypothesis (TCH) posits that the latitudinal gradient in biological diversity arises because most extant clades of animals and plants originated when tropical environments were more widespread and because the colonization of colder and more seasonal temperate environments is limited by the phylogenetically conserved environmental tolerances of these tropical clades. Recent studies have claimed support of the TCH, indicating that temperate plant diversity stems from a few more recently derived lineages that are nested within tropical clades, with the colonization of the temperate zone being associated with key adaptations to survive colder temperatures and regular freezing. Drought, however, is an additional physiological stress that could shape diversity gradients. Here, we evaluate patterns of evolutionary diversity in plant assemblages spanning the full extent of climatic gradients in North and South America. We find that in both hemispheres, extratropical dry biomes house the lowest evolutionary diversity, while tropical moist forests and many temperate mixed forests harbor the highest. Together, our results support a more nuanced view of the TCH, with environments that are radically different from the ancestral niche of angiosperms having limited, phylogenetically clustered diversity relative to environments that show lower levels of deviation from this niche. Thus, we argue that ongoing expansion of arid environments is likely to entail higher loss of evolutionary diversity not just in the wet tropics but in many extratropical moist regions as well.

Earth’s most studied biodiversity pattern is the latitudinal diversity gradient (LDG): species richness and evolutionary diversity decrease from the warm, moist, aseasonal tropics toward the colder, more seasonal poles (1–5). Many hypotheses have been proposed to explain the LDG (6), but the tropical conservatism hypothesis (TCH) has garnered much attention due to its focus on interacting ecological and evolutionary mechanisms (1, 2, 7–9) (Fig. 1A).Open in a separate windowFig. 1.A conceptual model of the distribution of evolutionary diversity across latitudinal and climatic gradients under two general mechanisms. (A) TCH—the latitudinal gradient is categorized into tropical or extratropical, and species richness is lower in extratropical regions because they comprise recently derived, evolutionarily poor (phylogenetically nested) subsets of lineages that have had less time for diversification relative to tropical lineages (i.e., lower evolutionary diversity in extratropical regions). The TCH is the prevalent mechanism addressed in studies of LDGs (e.g., ref. 2). (B) Extended TCH—the latitudinal gradient is categorized into four climatic domains: tropical moist, tropical dry, extratropical moist, or extratropical dry, and species richness is lower in extratropical moist, seasonally cold regions because they comprise recently derived, evolutionarily poor subsets of lineages relative to tropical assemblages. Within the tropics, species richness is lower in seasonally dry regions because they comprise recently derived, evolutionary poor subsets of lineages relative to tropical moist regions. Furthermore, extratropical dry regions, which exhibit both pronounced drought and cold temperatures, comprise recently derived, evolutionarily poor subsets of lineages relative to the other three climatic domains. Variation in evolutionary diversity differentiates regions with higher (positive values) or lower (negative) phylogenetic diversity than expected given their taxonomic diversity (e.g., species or generic richness). Thus, low values would indicate higher phylogenetic nestedness in these regions.The TCH makes two key assumptions: 1) that most clades of animals and plants have a tropical origin (3, 10, 11) and 2) that after the global cooling initiated at the end of the Eocene (34 Mya), the trait innovations necessary to persist and thrive in temperate regions (e.g., freezing tolerance) (12) are phylogenetically conserved within a small subset of more recently derived lineages (7, 12–14). Hence, the TCH predicts that relative to tropical regions, species richness in the temperate zone will be lower because temperate biodiversity stems from these few, more recently derived lineages that are phylogenetically nested within clades of tropical origin, and thus have had less time for diversification.While the inability of most plant lineages to survive regular freezing conditions clearly contributes to the LDG for flowering plants (2, 12), temperature may not be the sole stressor associated with the LDG. In particular, drought stress from either low precipitation (relative to evapotranspiration) or precipitation seasonality may have also disproportionately shaped diversity gradients (15, 16). Nonetheless, recent studies testing the validity of the TCH have ignored gradients of water availability in full (2) or have not included regions of extreme cold and drought in their analyses (17). Here, we evaluate an extended view of the TCH (8) (Fig. 1B). This view still assumes a tropical origin for most clades of extant species but generalizes the conservatism assumption such that the key innovations needed to thrive in any harsh or seasonal conditions, not just freezing temperatures, are limited to a few lineages.Under assumptions of the extended TCH, we would predict that any seasonally cold or dry environment will be made up of clusters of taxa within a few evolutionarily nested lineages of tropical origin. In these seasonal environments, we thus expect lower evolutionary diversity relative to regions that are aseasonal, warm, and wet year-round (henceforth, “tropical moist”).Although we make no assumptions regarding the age of extratropical dry environments, besides the TCH assumption of tropical moist origin for most clades of extant species (3, 10, 11), under the extended TCH, we would also predict that the number of lineages able to cope with more than one stressor is even more limited. This means that assemblages in extratropical dry regions exhibiting both pronounced drought and cold temperatures will consist of yet smaller subsets of lineages relative to environments that are either tropical moist or seasonal. In these extreme environments, we thus expect the lowest evolutionary diversity of any environment.To test the predictions of the extended TCH, we used a comprehensive dataset on the distribution of flowering plant species (angiosperms) across the Americas (18) and a time-scaled molecular phylogeny (12) for 3,847 angiosperm genera in the dataset. We then quantified species richness, phylogenetic diversity, and evolutionary diversity of plant assemblages a priori classified into one of 12 biomes (Fig. 2A) (19). Each assemblage represented a list of plant species contained within a 100 × 100 km grid cell, and the full extent of North and South America comprised 3,928 of these grid cells (hereafter “assemblages”). The species composition of the assemblages was derived from range maps available in BIEN (Botanical Information and Ecology Network; see Materials and Methods for further details). Evolutionary diversity was measured as the total phylogenetic branch length in an assemblage, standardized for the total number of genera in this assemblage, thus describing patterns of accumulated lineage diversity over evolutionary timescales—a metric we refer to as lineage diversity (LD; sensu ref. 16).Open in a separate windowFig. 2.Patterns of species richness (SR) and LD in angiosperm assemblages across the Americas. (A) Assemblages are classified into distinct biomes [following Olson et al. (19)]. (B) Geographical patterns of variation in SR for 3,928 angiosperm assemblages (sites). Each site is defined as the assemblage of angiosperm genera in a 100 × 100 km grid cell. Warmer colors indicate higher SR (i.e., the darkest red is assigned to the plant assemblage with SR = 8,924 species). Contours represent biome delimitations and are identical to contours in A. Dashed line indicates the Equator. (C) Geographical patterns of variation in LD for 3,928 angiosperm assemblages. LD was calculated as the total phylogenetic branch length in assemblages, standardized for genus-level richness. Warmer colors indicate higher LD (i.e., the darkest red is assigned to the plant assemblage with LD = 2.25 [sesPD]). (D) Distribution of LD values across biomes in the Americas, grouped by their climatic domain. Values represent 1,000 means of LD from 10 assemblages randomly selected within each biome. Colors of violin polygons are identical to A. Biomes are sorted by their median, and the dashed line indicates the highest median (i.e., temperate mixed forests). Values in parentheses after each biome name are the number of assemblages in that biome. Post hoc Dunn tests comparing pairwise biome means are provided in SI Appendix, Table S2. Refer to SI Appendix, Fig. S1 for a colorblind-friendly version of B and C.     

Clinical application of a new simple method for the identification of mucopolysaccharidoses

The clinical application of a new method for the quantitative determination of urinary glycosaminoglycans (GAGs) is presented. 115 normal subjects and 44 patients affected by different types of mucopolysaccharidoses (MPSo-ses) have been studied by this method in comparison with the conventional borate-carbazole method. All patients showed an urinary GAG excretion well above the normal subjects. In particular, patients affected by Morquio syndrome showed values well beyond the normal range; on the contrary, with the borate-carbazole method, 6 out of 7 patients had borderline values of urinary GAGs. The new method is also more rapid and easier to perform than conventional methods.