Evolutionary rates do not drive latitudinal diversity gradients

The topic of this thesis is the latitudinal diversity gradient: the general increase in numbers of species from high latitudes towards the equator. Although it is a well-documented and very general pattern, there is little consensus among biologists as to the causes of high tropical species richness. In Chapter 1 I give an overview of the latitudinal diversity gradient and hypotheses proposed to explain it, and outline a framework for developing and testing hypotheses. The emphasis in this thesis is on non-equilibrium hypotheses, and in particular on the idea that rates of species diversification are higher at low latitudes. In Chapter 2 I directly test the hypothesis that rates of species diversification increase towards the equator, using the phylogenetic method of sister-group comparisons. For birds and butterflies, 1 show that there does indeed appear to be an increase in rates of diversification towards lower latitudes. One possible explanation for this pattern links climatic conditions at low latitudes to faster speciation, via a causal chain which includes a higher rate of molecular evolution. In Chapter 3 I test the prediction that rates of molecular evolution are faster at low latitudes, using phylogenies reconstructed from DNA sequence data for birds. Although the results provide no evidence for a latitudinal effect on rates of cytb and ND2 evolution in birds, this chapter demonstrates a way in which further tests on a wider range of genes and taxa can be carried out as more sequence data becomes available. If rates of diversification are higher in the tropics, this may result from latitudinal gradients in life history traits which could influence rates of speciation or extinction. However, previous attempts to test for such patterns have rarely controlled for phylogenetic relationships among species, and have never controlled for geographic range overlap. In Chapter 4 I present a method for analyzing latitudinal variation in life history traits which takes both of these problems into account. For birds, this method indicates strong latitudinal variation in geographic range size and clutch size, less strong variation in body size and niche width, and no variation in the strength of sexual selection. While this does not prove that life history plays a part in generating the latitudinal diversity gradient, a robust demonstration of latitudinal variation in life history traits is an important prerequisite for any hypotheses which link life history with high tropical species richness. Speciation and extinction rates are believed to vary with species' life history and ecology. If speciation or extinction rates also vary with latitude, we should expect species with certain traits to show stronger latitudinal diversity gradients than others. We should also expect to see latitudinal variation in the macroecological structure of species assemblages. Chapters 5 and 6 confirm these expectations. In Chapter 5 I show that smaller-bodied bird species have steeper latitudinal diversity gradients than larger species. This is reflected in systematic latitudinal variation in the shape of body size frequency distributions, usually thought to be relatively consistent across regions. In Chapter 6 I show that body size - abundance relationships in the Australian marsupial fauna differ considerably between temperate and tropical subsets of the fauna. Whereas the temperate species display the typical negative relationship, the tropical species show no significant relationship. This pattern is consistent with the explanation that extinction rates vary with respect to body size, abundance and the latitude in which a species occurs. Together, the results of the analyses presented in this thesis provide evidence in favour of the non-equilibrium view that there are more species in the tropics because rates of species diversification are higher. It seems likely that this is due to latitudinal variation in environmental conditions, leading to latitudinal variation in species' life histories and the structure of species assemblages, and to latitudinal variation in rates of speciation or extinction. However, it is still difficult to judge whether it is variation in speciation rate (cradle model) or extinction rate (museum model) which is of primary importance, or if both are equally important. Further work on this question, applying the large-scale comparative methodology used here, will be necessary to progress towards a full understanding of the high species richness of the tropics.

The latitudinal diversity gradient (LDG) refers to a decrease in biodiversity from the equator to the poles. The evolutionary speed hypothesis, backed by the metabolic theory of ecology, asserts that nucleotide mutation and substitution rates per site per year are higher and thereby speciation rates are higher at higher temperatures, generating the LDG. However, prior empirical investigations of the relationship between the temperature and mutation or substitution rate were based on a few genes and the results were mixed. We here revisit this relationship using genomic data. No significant correlation between the temperature and mutation rate is found in 13 prokaryotes or in 107 eukaryotes. An analysis of 234 diverse trios of bacterial taxa indicates that the synonymous substitution rate is not significantly associated with the growth temperature. The same data, however, reveal a significant negative association between the nonsynonymous substitution rate and temperature, which is explainable by a larger fraction of detrimental nonsynonymous mutations at higher temperatures due to a stronger demand for protein stability. We conclude that the evolutionary speed hypothesis of the LDG is unsupported by genomic data and advise that future mechanistic studies of the LDG should focus on other hypotheses.

The role of historical factors in driving latitudinal diversity gradients is poorly understood. Here, we used an updated global phylogeny of terrestrial birds to test the role of three key historical factors-speciation, extinction, and dispersal rates-in generating latitudinal diversity gradients for eight major clades. We fit a model that allows speciation, extinction, and dispersal rates to differ, both with latitude and between the New and Old World. Our results consistently support extinction (all clades had lowest extinction where species richness was highest) as a key driver of species richness gradients across each of eight major clades. In contrast, speciation and dispersal rates showed no consistent latitudinal patterns across replicate bird clades, and thus are unlikely to represent general underlying drivers of latitudinal diversity gradients.

We still have much to learn about the evolution of taxonomic diversity gradients through geologic time. For example, have latitudinal gradients always been as steep as they are now, or is this a phenomenon linked to some form of Cenozoic global climatic differentiation? The fossil record offers potential to address this sort of problem, and this study reconstructs latitudinal diversity gradients for the last (Tithonian) stage of the Jurassic period using marine bivalves. At this time of relative global warmth, bivalves were cosmopolitan in their distribution and the commonest element within macrobenthic assemblages.Analysis of 31 regional bivalve faunas demonstrates that Tithonian latitudinal gradients were present in both hemispheres, though on a much smaller magnitude than today. The record of the Northern Hemisphere gradient is more complete and shows a steep fall in values at the tropical/temperate boundary; the Southern Hemisphere gradient exhibits a more regular decline in diversity with increasing latitude.Tithonian latitudinal gradients were underpinned by a tropical bivalve fauna that comprises almost equal numbers of epifaunal and infaunal taxa. The epifaunal component was dominated by three pteriomorph families, the Pectinidae, Limidae and Ostreidae, that may be regarded as a long-term component of tropical bivalve diversity. Of the mixture of older and newer “heteroconch” families that formed the bulk of the infaunal component, the latter radiated spectacularly through the Late Cretaceous and Cenozoic to dominate tropical bivalve faunas at the present day. This pulse of heteroconch diversification, which was a major cause of the steepening of the bivalve latitudinal gradient, provides important evidence that rates of speciation may be negatively correlated with latitude.Nevertheless, we cannot exclude the possibility that elevated extinction rates in the highest latitudes also contributed to the marked steepening of bivalve latitudinal gradients over the last 150 Myr. Rates of extinction within epifaunal bivalve taxa appear to have been higher in these regions through the Cretaceous period, but this was largely before any significant global climatic deterioration. Infaunal bivalve clades have had differential success over this time period in the polar regions. Whereas, in comparison with the Tropics, heteroconchs are very much reduced in numbers today, the anomalodesmatans are much better represented, and the protobranchs have positively thrived. We are beginning to appreciate that low temperature per se may not be a primary cause of elevated rates of extinction. Food supply may be an equally important control on both rates of speciation and extinction; those bivalves that have been able to adapt to the extreme seasonality of food supply have flourished in the polar regions.

Ecology's oldest pattern?

Evolutionary origin of the latitudinal diversity gradient in liverworts

Species diversity patterns are governed by complex interactions among biotic and abiotic factors over time and space, but are essentially the result of the diversification dynamics (differential speciation and extinction rates) over the long‐term evolutionary history of a clade. Previous studies have suggested that temporal variation in global temperature drove long‐term diversity changes in Crocodylia, a monophyletic group of large ectothermic organisms. We use a large database of crocodylian fossil occurrences (192 spp.) and body mass estimations, under a taxic approach, to characterize the global diversification dynamics of crocodylians since the Cretaceous, and their correlation with multiple biotic and abiotic factors in a Bayesian framework. The diversification dynamic of crocodylians, which appears to have originated in the Turonian (c. 92.5 Ma), is characterized by several phases with high extinction and speciation rates within a predominantly low long‐term mean rate. Our results reveal long‐term diversification dynamics of Crocodylia to be a highly complex process driven by a combination of biotic and abiotic factors which influenced the speciation and extinction rates in dissimilar ways. Higher crocodylian extinction rates are related to low body mass disparity, indicating selective extinctions of taxa at both ends of the body mass spectrum. Speciation rate slowdowns are noted when the diversity of the clade is high and the warm temperate climatic belt is reduced. Our finding supports the idea that temporal variations of body mass disparity, self‐diversity, and the warm climate belt size provided more direct mechanistic explanations for crocodylian diversification than do proxies of global temperature.

An impediment to understanding the origin and dynamics of the latitudinal diversity gradient (LDG)-the most pervasive large-scale biotic pattern on Earth-has been the tendency to focus narrowly on a single causal factor when a more synthetic, integrative approach is needed. Using marine bivalves as a model system and drawing on other systems where possible, we review paleobiologic and biogeographic support for two supposedly opposing views, that the LDG is shaped primarily by (a) local environmental factors that determine the number of species and higher taxa at a given latitude (in situ hypotheses) or (b) the entry of lineages arising elsewhere into a focal region (spatial dynamics hypotheses). Support for in situ hypotheses includes the fit of present-day diversity trends in many clades to such environmental factors as temperature and the correlation of extinction intensities in Pliocene bivalve faunas with net regional temperature changes. Support for spatial dynamics hypotheses includes the age-frequency distribution of bivalve genera across latitudes, which is consistent with an out-of-the-tropics dynamic, as are the higher species diversities in temperate southeastern Australia and southeastern Japan than in the tropical Caribbean. Thus, both in situ and spatial dynamics processes must shape the bivalve LDG and are likely to operate in other groups as well. The relative strengths of the two processes may differ among groups showing similar LDGs, but dissecting their effects will require improved methods of integrating fossil data with molecular phylogenies. We highlight several potential research directions and argue that many of the most dramatic biotic patterns, past and present, are likely to have been generated by diverse, mutually reinforcing drivers.

Global trophic ecology of yellowfin, bigeye, and albacore tunas: Understanding predation on micronekton communities at ocean-basin scales

AimThe pattern of increasing biological diversity from high latitudes to the equator [latitudinal diversity gradient (LDG)] has been recognized for > 200 years. Empirical studies have documented this pattern across many different organisms and locations. Our goal was to quantify the evidence for the global LDG and the associated spatial, taxonomic and environmental factors. We performed a meta‐analysis on a large number of individual LDGs that have been published in the 14 years since Hillebrand's ground‐breaking meta‐analysis of the LDG, using meta‐analysis and meta‐regression approaches largely new to the fields of ecology and biogeography.LocationGlobal.Time periodJanuary 2003–September 2015.Major taxa studiedBacteria, protists, plants, fungi and animals.MethodsWe synthesized the outcomes of 389 individual cases of LDGs from 199 papers published since 2003, using hierarchical mixed‐effects meta‐analysis and multiple meta‐regression. Additionally, we re‐analysed Hillebrand's original dataset using modern methods.ResultsWe confirmed the generality of the LDG, but found the pattern to be weaker than was found in Hillebrand's study. We identified previously unreported variation in LDG strength and slope across longitude, with evidence that the LDG is strongest in the Western Hemisphere. Locational characteristics, such as habitat and latitude range, contributed significantly to LDG strength, whereas organismal characteristics, including taxonomic group and trophic level, did not. Modern meta‐analytical models that incorporate hierarchical structure led to more conservative and sometimes contrasting effect size estimates relative to Hillebrand's initial analysis, whereas meta‐regression revealed underlying patterns in Hillebrand's dataset that were not apparent with a traditional analysis.Main conclusionsWe present evidence of global latitudinal, longitudinal and habitat‐based patterns in the LDG, which are apparent across both marine and terrestrial realms and over a broad taxonomic range of organisms, from bacteria to plants and vertebrates.

A well-documented pattern in the fossil record is a long-term decline in the origination rate of new taxa after diversity rebounds from a mass extinction. The mechanisms for this pattern remain elusive. In this article, we investigate the macroevolutionary predictions of an individual-based birth-death model (BDI model) where speciation and extinction rates emerge from population dynamics. We start with the simplest neutral model in which every individual has the same per capita rates of birth, death, and speciation. Although the prediction of the simplest neutral model agrees qualitatively with the fossil pattern, the predicted decline in per-species speciation rates is too fast to explain the long-term trend in fossil data. We thus consider models with variation among species in per capita rates of speciation and a suite of alternative assumptions about the heritability of speciation rate. The results show that interspecific variation in per capita speciation rate can induce differences among species in their ability to resist extinction because a low speciation rate confers a small but important demographic advantage. As a consequence, the model predicts an appropriately slow temporal decline in speciation rates, which provides a mechanistic explanation for the fossil pattern.

ObjectivesThis study examines how speciation and extinction rates vary across primates, with a focus on the recent macroevolutionary dynamics that have shaped extant primate biodiversity.Materials and methodsLineage‐specific macroevolutionary rates were estimated for each tip in a tree containing 307 species using a hidden‐state likelihood model. Differences in tip rates among major clades were evaluated using phylogenetic ANOVA. Differences among diurnal, nocturnal, and cathemeral lineages were also evaluated, based on previous work indicating that activity pattern influences primate diversification.ResultsRate variation in extant primates is low within clades and high between clades. As in previous studies, cercopithecoids stand out in having high net diversification rates, driven by high speciation rates and very low extinction rates. Platyrrhines combine high speciation and high extinction rates, giving them high rates of lineage turnover. Strepsirrhines and tarsiids have low rates of speciation, extinction, turnover, and net diversification. Hominoids are intermediate between platyrrhines and the strepsirrhine‐tarsiid group, and there is evidence for differentiation between hominids and hylobatids. Diurnal lineages have significantly higher speciation rates than nocturnal lineages.ConclusionsRecent anthropoid macroevolution has been characterized by marked variation in diversification dynamics among clades. Strepsirrhines and tarsiids are more uniform, despite divergent evolutionary and biogeographic histories. Higher speciation rates in diurnal lineages may be driven by greater ecological opportunity or reliance on visual signals for mate recognition. However, the differences among anthropoids indicate that factors other than activity pattern (e.g., clade competition, historical contingency) have had a more influential role in shaping recent primate diversification.

Speciation and extinction rates can be estimated from molecular phylogenies. Recently, a number of methods have been published showing that these rates can be estimated even if the phylogeny is incomplete, that is, if not all extant species are included. We show that the accuracy of such methods strongly depends on making the correct assumptions about how the sampling process was performed. We focus on phylogenies that are incomplete because some subclades (e.g., genera and families) are each represented as a single lineage. We show that previous methods implicitly assumed that such subclades are defined by randomly (or in an extreme deterministic way) choosing the edges that define the subclades from the complete species phylogeny. We show that these methods produce biased results if higher taxa are defined in a different manner. We introduce strict higher level phylogenies where subclades are defined so that the phylogeny is fully resolved from its origin to time x(cut), and fully unresolved thereafter, so that for all subclades, stem age > x(cut) > crown age. We present estimates of speciation and extinction rates from a phylogeny of birds in which this subclade definition was applied. However, for most higher level phylogenies in the literature, it is unclear how higher taxa were defined, but often such phylogenies can be easily transformed into strict higher level phylogenies, as we illustrate by estimating speciation and extinction rates from a near-complete but only partly resolved species-level phylogeny of mammals. The accuracy of our methods is verified using simulations.

The latitudinal diversity gradient (LDG) is a widely recognized biogeographic pattern, yet its persistence under increasing human impacts remains unclear. Leveraging 17 million eBird records, we investigated how urbanization alters LDGs in North America. We quantified LDGs across 662 cities and their surroundings, and found that LDGs vary by season and native status: non-native species exhibited weak or no LDG, whereas native birds showed the strongest LDG during winter. Notably, native birds showed a significantly flatter winter LDG in cities than in surrounding areas. Although human population density generally reduced bird diversity, it exerted positive effects under cold conditions in high latitudes. These findings indicate that urbanization can reshape classic biodiversity patterns, with cities potentially acting as winter refuges for native birds at higher latitudes.

Recently, studies about the spatial distribution of microbial species and communities have increased substantially. Freshwater diatoms are used as one of the most popular model taxa in such macroecological studies, but the most exciting patterns in the spatial ecology of diatoms have not been reviewed. Here, we identify 15 important questions about freshwater diatom ecology, review the major findings, and suggest novel research avenues. We found that diatoms do not support classical latitudinal diversity gradient, species–area relationship or Rapoport's rule. We found some, albeit inconsistent support for an elevational diversity gradient, Bergmann's rule and niche conservation. Diatoms do support a positive interspecific abundance–occupancy relationship like nearly all other taxa. With regards to metacommunity dynamics, diatom communities are typically structured by species sorting, but neutral dynamics or mass effects are also evident at large or small spatial scale, respectively. Taken together, this review suggests that diatoms follow some classical biogeographical patterns similarly to larger taxa, but patterns are typically weaker than for macro‐organisms. This may result because diatoms are typically relatively strongly controlled by local factors and often exhibit efficient stochastic dispersal processes both at small and large scales. More research is needed to build a more comprehensive view of diatom species–area relationships and latitudinal gradients in diversity, for example. In the future, well‐replicated macroecological field experiments, diatom studies with intercontinental or global coverage, trait‐based approaches, and DNA‐based species identification would be fruitful avenues to shed more light into the spatial ecology of diatoms.