Origins of marine patterns of biodiversity: some correlates and applications

Abstract: Marine shelf diversity patterns correlate with macroecological features of basic importance that may play causal roles in macroevolution. We have investigated the global diversity pattern of living Bivalvia, which is dominated by the latitudinal diversity gradient (LDG), maintained by high tropical origination rates. Generic‐level lineages expand poleward, chiefly through speciation, so that species richness within provinces and globally is positively correlated with generic geographical ranges. A gradient in diversity accommodation progressively lowers both immigration and speciation rates in higher latitudes. The LDG correlates with seasonality of trophic resources but not with area; tropical provinces are not diverse because they are large but because they are tropical. A similar dynamic evidently underlays Jurassic and Carboniferous LDGs. Larval developmental modes correlate with the LDG and thus with resource seasonality, with tropical dominance of planktotrophs offset by increasing nonplanktotrophy to poleward. The acquisition of planktotrophy in several early Palaeozoic clades indicates a change in macroecological relationships during Cambrian and Ordovician radiations.     

Latitudinal‐diversity gradients can be shaped by biotic processes: new insights from an eco‐evolutionary model

The processes involved in shaping latitudinal‐diversity gradients (LDGs) have been a longstanding source of debate and research. Climatic, historical and evolutionary factors have all been shown to contribute to the formation of LDGs. However, meta‐analyses have shown that different clades have LDG slopes that may vary in more than one order of magnitude. Such large variation cannot be explained solely by climatic or historical factors (e.g. difference in surface area between temperate and tropical zones) given that all clades within a geographic region are subject to the same conditions. Therefore, biotic processes intrinsic to each taxonomic group could be relevant in explaining rate differences in diversity decline across latitudinal gradients among groups. In this study, we developed a model simulating multiple competing species subjected (or not) to a demographic Allee effect. We simulated the range expansion of these species across an environmental gradient to show how these two overlooked factors (competition and Allee effects) are capable of modulating LDGs. Allee effects resulted in a steeper LDG given a higher probability of local extinction and lower colonization capacity compared to species without Allee effects. Likewise, stronger competition also led to a steeper decline in species diversity compared to scenarios with weaker species antagonistic interactions. This pattern occurred mostly due to the strength of priority effects, wherein scenarios with strong competition, species that dispersed earlier in the landscape were able to secure many patches whereas late‐arriving species were progressively precluded from expanding their ranges. Overall, our results suggest that the effect of biotic processes in shaping macroecological patterns could be more important than it is currently appreciated.     

Environmental harshness,latitude and incipient speciation

Are rates of evolution and speciation fastest where diversity is greatest – the tropics? A commonly accepted theory links the latitudinal diversity gradient to a speciation pump model whereby the tropics produce species at a faster rate than extra‐tropical regions. In this issue of Molecular Ecology, Botero et al. ( 2014 ) test the speciation pump model using subspecies richness patterns for more than 9000 species of birds and mammals as a proxy for incipient speciation opportunity. Rather than using latitudinal centroids, the authors investigate the role of various environmental correlates of latitude as drivers of subspecies richness. Their key finding points to environmental harshness as a positive predictor of subspecies richness. The authors link high subspecies richness in environmental harsh areas to increased opportunities for geographic range fragmentation and/or faster rates of trait evolution as drivers of incipient speciation. Because environmental harshness generally increases with latitude, these results suggest that opportunity for incipient speciation is lowest where species richness is highest. The authors interpret this finding as incompatible with the view of the tropics as a cradle of diversity. Their results are consistent with a growing body of evidence that reproductive isolation and speciation occur fastest at high latitudes.     

Open science and meta‐analysis allow for rapid advances in ecology: A response to Menegotto et al. (2019)

Menegotto and colleagues’ (2019) commentary on our paper (Kinlock et al., 2018) does not negate our findings, but by recategorizing and reanalysing a portion of our data set, advances our knowledge of the latitudinal diversity gradients (LDGs) in marine ecosystems, particularly emphasizing different findings for benthic LDGs as a result of the recategorization of the data. Furthermore, we see the contribution by Menegotto et al. (2019) as highlighting the importance of scientific transparency; we believe that this insight into the nature of LDGs in marine systems would have been delayed, if not unobtainable, had we not provided fully transparent methods and complete data in our paper.     

Extinction as a driver of avian latitudinal diversity gradients

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.     

The tropics: cradle,museum or casino? A dynamic null model for latitudinal gradients of species diversity

Several ecological and evolutionary hypotheses have been proposed to explain the latitudinal diversity gradient (LDG), but a general model for this conspicuous pattern remains elusive. Mid-domain effect (MDE) models generate gradients of species diversity by randomly placing the geographic ranges of species in one- or two-dimensional spaces, thus excluding both evolutionary processes and the effect of contemporary climate. Traditional MDE models are statistical and static because they determine the size of ranges either randomly or based on empirical frequency distributions. Here we present a simple dynamic null model for the LDG that simulates stochastic processes of range shifts, extinction and speciation. The model predicts higher species diversity and higher extinction and speciation rates in the tropics, and a strong influence of range movements in shaping the LDG. These null expectations should be taken into consideration in studies aimed at understanding the many factors that generate latitudinal diversity gradients.     

Can the tropical conservatism hypothesis explain temperate species richness patterns? An inverse latitudinal biodiversity gradient in the New World snake tribe Lampropeltini

Aim  A latitudinal gradient in species richness, defined as a decrease in biodiversity away from the equator, is one of the oldest known patterns in ecology and evolutionary biology. However, there are also many known cases of increasing poleward diversity, forming inverse latitudinal biodiversity gradients. As only three processes (speciation, extinction and dispersal) can directly affect species richness in areas, similar factors may be responsible for both classical (high tropical diversity) and inverse (high temperate diversity) gradients. Thus, a modified explanation for differential species richness which accounts for both patterns would be preferable to one which only explains high tropical biodiversity.
Location  The New World.
Methods  We test several proposed ecological, temporal, evolutionary and spatial explanations for latitudinal diversity gradients in the New World snake tribe Lampropeltini, which exhibits its highest biodiversity in temperate regions.
Results  We find that an extratropical peak in species richness is not explained by latitudinal variation in diversification rate, the mid-domain effect, or Rapoport's rule. Rather, earlier colonization and longer duration in the temperate zones allowing more time for speciation to increase biodiversity, phylogenetic niche conservatism limiting tropical dispersal and the expansion of the temperate zones in the Tertiary better explain inverse diversity gradients in this group.
Main conclusions  Our conclusions are the inverse of the predictions made by the tropical conservatism hypothesis to explain higher biodiversity near the equator. Therefore, we suggest that the processes invoked are not intrinsic to the tropics but are dependent on historical biogeography to determine the distribution of species richness, which we refer to as the 'biogeographical conservatism hypothesis'.     

Diversification rates and the latitudinal gradient of diversity in mammals

The latitudinal gradient of species richness has frequently been attributed to higher diversification rates of tropical groups. In order to test this hypothesis for mammals, we used a set of 232 genera taken from a mammalian supertree and, additionally, we reconstructed dated Bayesian phylogenetic trees of 100 genera. For each genus, diversification rate was estimated taking incomplete species sampling into account and latitude was assigned considering the heterogeneity in species distribution ranges. For both datasets, we found that the average diversification rate was similar among all latitudinal bands. Furthermore, when we used phylogenetically independent contrasts, we did not find any significant correlation between latitude and diversification parameters, including different estimates of speciation and extinction rates. Thus, other factors, such as the dynamics of dispersal through time, may be required to explain the latitudinal gradient of diversity in mammals.     

Climatic control of dispersal–ecological specialization trade‐offs: a metacommunity process at the heart of the latitudinal diversity gradient?

We outline the potentially important role of dispersal in linking diversity patterns at different spatial and temporal scales, and the resulting potential to link hypotheses explaining macroscale patterns of diversity. We do this by proposing a possible mechanism linking climate to diversity patterns: we argue that climate, via effects of continuity of habitat availability in space and time, mediates a dispersal–ecological specialization trade‐off at the metacommunity level that leads to latitudinal trends in dispersal ability, ecological specialization, range sizes, speciation and species richness, ultimately driving the latitudinal diversity gradient. This trade‐off constitutes a possible mechanism for the strong macroscale correlation between climate and species richness that is consistent with recent ideas about niche conservatism and gradient lengths, as well as other leading hypotheses. We present an overview of predictions derived from our ideas. Of these, some have already been tested and supported and others are still open to debate or need testing. Together they provide a unique set of predictions that allows falsification.     

Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography

A latitudinal gradient in biodiversity has existed since before the time of the dinosaurs, yet how and why this gradient arose remains unresolved. Here we review two major hypotheses for the origin of the latitudinal diversity gradient. The time and area hypothesis holds that tropical climates are older and historically larger, allowing more opportunity for diversification. This hypothesis is supported by observations that temperate taxa are often younger than, and nested within, tropical taxa, and that diversity is positively correlated with the age and area of geographical regions. The diversification rate hypothesis holds that tropical regions diversify faster due to higher rates of speciation (caused by increased opportunities for the evolution of reproductive isolation, or faster molecular evolution, or the increased importance of biotic interactions), or due to lower extinction rates. There is phylogenetic evidence for higher rates of diversification in tropical clades, and palaeontological data demonstrate higher rates of origination for tropical taxa, but mixed evidence for latitudinal differences in extinction rates. Studies of latitudinal variation in incipient speciation also suggest faster speciation in the tropics. Distinguishing the roles of history, speciation and extinction in the origin of the latitudinal gradient represents a major challenge to future research.     

Marine longitudinal biodiversity: causes and conservation

The horizontal temperature zones of the earth tend to restrict the latitudinal ranges of species but allow the possibility of exceedingly broad longitudinal dispersals. In the Tropical Zone, biodiversity on the continental shelves is not homogeneous but is concentrated in two conspicuous peaks, one in the Indo‐Pacific Ocean and the other in the Atlantic. The Indo‐Pacific biodiversity peak is located within a relatively small area called the East Indies Triangle. The Atlantic peak is located in the southern Caribbean Sea. Evidence that has been accumulated over the years indicates that each area functions as a centre of origin and evolutionary radiation. What are the causes of these concentrations and their present functions? A newly published model indicates a positive relationship between environmental temperature and the rate of speciation. While this helps to explain the generally high tropical diversity, and the negative relationship between diversity and latitude, it does not provide a reason for the longitudinal concentrations. But, other new research serves to substantiate previous indications of a positive relationship between speciation rate and species diversity. The existence of this positive feedback, together with some contributory factors, provides the reason why concentrations occur. The evolutionary radiation probably begins when the build‐up of species diversity reaches a critical level. The warm‐temperate biotas are derived from the tropics. Their northern longitudinal relationships tend to be minor but, in the southern hemisphere, the West Wind Drift is an important dispersal mechanism for both warm‐temperate and cold‐temperate species. The cold‐temperate biotas peaked in two areas, the North Pacific and the Antarctic; each has developed into a centre of origin. The continuous dispersal of well‐adapted species from the centres helps peripheral communities maintain diversity.     

Latitudinal gradients in diversity: real patterns and random models

Mid-domain models have been argued lo provide a default explanation for the best known spatial pattern in biodiversity, namely the latitudinal gradient in species richness. These models assume no environmental gradients, but merely a random latitudinal association between the size and placement of the geographic ranges of species. A mid-domain peak in richness is generated because when the latitudinal extents of species in a given taxonomic group are bounded to north and south, perhaps by a physical constraint such as a continental edge or perhaps by a climatic constraint such as a critical temperature or precipitation threshold, then the number of ways in which ranges can be distributed changes systematically between the bounds. In addition, such models make predictions about latitudinal variation in the latitudinal extents of the distributions of species, and in beta diversity (the spatial turnover in species identities). Here we test how well five mid-domain models predict observed latitudinal patterns of species richness, latitudinal extent and beta diversity in two groups of birds, parrots and woodpeckers, across the New World. Whilst both groups exhibit clear gradients in richness and beta diversity and the general trend in species richness is acceptably predicted (but not accurately, unless substantial empirical information is assumed), the fit of these models is uniformly poor for beta diversity and latitudinal range extent. This suggests either that, at least for these data, as presently formulated mid-domain models are too simplistic, or that in practice the mid-domain effect is not significant in determining geographical variation in diversity.     

Evidence for a time-integrated species-area effect on the latitudinal gradient in tree diversity

The greater area of tropical forest biomes has been proposed as a factor that drives the latitudinal gradient in species diversity by modulating speciation and extinction rates. But speciation and extinction are processes that operate over millions of years, so an adequate test of area's contribution to diversity patterns must take into consideration that biome areas have changed through time in response to climate. Here we correlate estimates of current tree species diversity with a composite parameter integrating area over geological time for each continent's tropical, temperate, and boreal biomes. We find significant positive correlations between current tree diversity and area-time for periods since the Eocene, Oligocene, and Miocene, which we take as evidence for a time-integrated species-area effect on current patterns of species richness across biomes. These results contribute to explanations for why most lineages have tropical origins and why tropical forests are more diverse than extratropical forests.     

Testing the link between the latitudinal gradient in species richness and rates of molecular evolution

Numerous hypotheses have been proposed to explain latitudinal gradients in species richness, but all are subject to ongoing debate. Here we examine Rohde's (1978, 1992) hypothesis, which proposes that climatic conditions at low latitudes lead to elevated rates of speciation. This hypothesis predicts that rates of molecular evolution should increase towards lower latitudes, but this prediction has never been tested. We discuss potential links between rates of molecular evolution and latitudinal diversity gradients, and present the first test of latitudinal variation in rates of molecular evolution. Using 45 phylogenetically independent, latitudinally separated pairs of bird species and higher taxa, we compare rates of evolution of two mitochondrial genes and DNA-DNA hybridization distances. We find no support for an effect of latitude on rate of molecular evolution. This result casts doubt on the generality of a key component of Rohde's hypothesis linking climate and speciation.     

What causes latitudinal gradients in species diversity? Evolutionary processes and ecological constraints on swallowtail biodiversity

The latitudinal diversity gradient (LDG) is one of the most striking ecological patterns on our planet. Determining the evolutionary causes of this pattern remains a challenging task. To address this issue, previous LDG studies have usually relied on correlations between environmental variables and species richness, only considering evolutionary processes indirectly. Instead, we use a phylogenetically integrated approach to investigate the ecological and evolutionary processes responsible for the global LDG observed in swallowtail butterflies (Papilionidae). We find evidence for the 'diversification rate hypothesis' with different diversification rates between two similarly aged tropical and temperate clades. We conclude that the LDG is caused by (1) climatically driven changes in both clades based on evidence of responses to cooling and warming events, and (2) distinct biogeographical histories constrained by tropical niche conservatism and niche evolution. This multidisciplinary approach provides new findings that allow better understanding of the factors that shape LDGs.     

Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity

Many groups show higher species richness in tropical regions but the underlying causes remain unclear. Despite many competing hypotheses to explain latitudinal diversity gradients, only three processes can directly change species richness across regions: speciation, extinction and dispersal. These processes can be addressed most powerfully using large-scale phylogenetic approaches, but most previous studies have focused on small groups and recent time scales, or did not separate speciation and extinction rates. We investigate the origins of high tropical diversity in amphibians, applying new phylogenetic comparative methods to a tree of 2871 species. Our results show that high tropical diversity is explained by higher speciation in the tropics, higher extinction in temperate regions and limited dispersal out of the tropics compared with colonization of the tropics from temperate regions. These patterns are strongly associated with climate-related variables such as temperature, precipitation and ecosystem energy. Results from models of diversity dependence in speciation rate suggest that temperate clades may have lower carrying capacities and may be more saturated (closer to carrying capacity) than tropical clades. Furthermore, we estimate strikingly low tropical extinction rates over geological time scales, in stark contrast to the dramatic losses of diversity occurring in tropical regions presently.     

Sexual selection and speciation: the comparative evidence revisited

The spectacular diversity in sexually selected traits in the animal kingdom has inspired the hypothesis that sexual selection can promote species divergence. In recent years, several studies have attempted to test this idea by correlating species richness with estimates of sexual selection across phylogenies. These studies have yielded mixed results and it remains unclear whether the comparative evidence can be taken as generally supportive. Here, we conduct a meta‐analysis of the comparative evidence and find a small but significant positive overall correlation between sexual selection and speciation rate. However, we also find that effect size estimates are influenced by methodological choices. Analyses that included deeper phylogenetic nodes yielded weaker correlations, and different proxies for sexual selection showed different relationships with species richness. We discuss the biological and methodological implications of these findings. We argue that progress requires more representative sampling and justification of chosen proxies for sexual selection and speciation rate, as well as more mechanistic approaches.     

Southern hospitality: a latitudinal gradient in gene flow in the marine environment

In recent years population genetics and phylogeographic studies have become increasingly valuable tools for inferring both historical and present-day genetic patterns within marine species. Here, we take a comparative approach to population-level study, analyzing original mitochondrial DNA data from 969 individuals representing 28 chiton (Mollusca: Polyplacophora) species to uncover large-scale genetic patterns along the Pacific coast of North America. The data reveal a distinct latitudinal connectivity gradient among chitons: species that exist at lower latitudes tend to have more isolated populations. This trend appears to be a product of between-species differences; within species, no significant gradient in connectivity is observed. Lower average annual sea surface temperatures are hypothesized to contribute to longer larval duration (and by extension, greater connectivity) among lecithotrophic species, providing a mechanism for the observed positive correlation between gene flow and latitude. Because increased isolation among populations may lead to speciation, a latitudinal trend in gene flow may contribute to the increased species diversity observed at lower latitudes.     

EVOLUTIONARY AND BIOGEOGRAPHIC ORIGINS OF HIGH TROPICAL DIVERSITY IN OLD WORLD FROGS (RANIDAE)

Differences in species richness between regions are ultimately explained by patterns of speciation, extinction, and biogeographic dispersal. Yet, few studies have considered the role of all three processes in generating the high biodiversity of tropical regions. A recent study of a speciose group of predominately New World frogs (Hylidae) showed that their low diversity in temperate regions was associated with relatively recent colonization of these regions, rather than latitudinal differences in diversification rates (rates of speciation–extinction). Here, we perform parallel analyses on the most species-rich group of Old World frogs (Ranidae; ∼1300 species) to determine if similar processes drive the latitudinal diversity gradient. We estimate a time-calibrated phylogeny for 390 ranid species and use this phylogeny to analyze patterns of biogeography and diversification rates. As in hylids, we find a strong relationship between the timing of colonization of each region and its current diversity, with recent colonization of temperate regions from tropical regions. Diversification rates are similar in tropical and temperate clades, suggesting that neither accelerated tropical speciation rates nor greater temperate extinction rates explain high tropical diversity in this group. Instead, these results show the importance of historical biogeography in explaining high species richness in both the New World and Old World tropics.