Diversity across organisational scale emerges through dispersal ability and speciation dynamics in tropical fish.

BACKGROUND: Biodiversity exists at different levels of organisation: e.g. genetic, individual, population, species, and community. These levels of organisation all exist within the same system, with diversity patterns emerging across organisational scales through several key processes. Despite this inherent interconnectivity, observational studies reveal that diversity patterns across levels are not consistent and the underlying mechanisms for variable continuity in diversity across levels remain elusive. To investigate these mechanisms, we apply a spatially explicit simulation model to simulate the global diversification of tropical reef fishes at both the population and species levels through emergent population-level processes. RESULTS: We find significant relationships between the population and species levels of diversity which vary depending on both the measure of diversity and the spatial partitioning considered. In turn, these population-species relationships are driven by modelled biological trait parameters, especially the divergence threshold at which populations speciate. CONCLUSIONS: To explain variation in multi-level diversity patterns, we propose a simple, yet novel, population-to-species diversity partitioning mechanism through speciation which disrupts continuous diversity patterns across organisational levels. We expect that in real-world systems this mechanism is driven by the molecular dynamics that determine genetic incompatibility, and therefore reproductive isolation between individuals. We put forward a framework in which the mechanisms underlying patterns of diversity across organisational levels are universal, and through this show how variable patterns of diversity can emerge through organisational scale.

Elevational Goldilocks zone underlies the exceptional diversity of a large lizard radiation (Liolaemus; Liolaemidae).

Mountains are among the most biodiverse regions on the planet, and how these landforms shape diversification through the interaction of biological traits and geo-climatic dynamics is integral to understanding global biodiversity. In this study, we investigate the dual roles of climate change and mountain uplift on the evolution of a hyper-diverse radiation, Liolaemus lizards, with a spatially explicit model of diversification using a reconstruction of uplift and paleotemperature in central and southern South America. The diversification model captures a hotspot for Liolaemus around 40°S in lineages with low-dispersal ability and narrow niche breadths. Under the model, speciation rates are highest in low latitudes (<35°S) and mid elevations (~1,000 m), while extinction rates are highest at higher latitudes (>35°S) and higher elevations (>2,000 m). Temperature change through the Cenozoic explained variation in speciation and extinction rates through time and across different elevational bands. Our results point to the conditions of mid elevations being optimal for diversification (i.e., Goldilocks Zone), driven by the combination of (1) a complex topography that facilitates speciation during periods of climatic change, and (2) a relatively moderate climate that enables the persistence of ectothermic lineages and buffers species from extinction.

The geography of climate and the global patterns of species diversity.

Climate's effect on global biodiversity is typically viewed through the lens of temperature, humidity and resulting ecosystem productivity1-6. However, it is not known whether biodiversity depends solely on these climate conditions, or whether the size and fragmentation of these climates are also crucial. Here we shift the common perspective in global biodiversity studies, transitioning from geographic space to a climate-defined multidimensional space. Our findings suggest that larger and more isolated climate conditions tend to harbour higher diversity and species turnover among terrestrial tetrapods, encompassing more than 30,000 species. By considering both the characteristics of climate itself and its geographic attributes, we can explain almost 90% of the variation in global species richness. Half of the explanatory power (45%) may be attributed either to climate itself or to the geography of climate, suggesting a nuanced interplay between them. Our work evolves the conventional idea that larger climate regions, such as the tropics, host more species primarily because of their size7,8. Instead, we underscore the integral roles of both the geographic extent and degree of isolation of climates. This refined understanding presents a more intricate picture of biodiversity distribution, which can guide our approach to biodiversity conservation in an ever-changing world.

Priorities for conserving the world's terrestrial mammals based on over-the-horizon extinction risk.

Three major axes of global change put the world's mammal biodiversity at risk: climate change, human population growth, and land-use change.1,2,3,4,5,6,7,8,9,10,11,12 In some parts of the world the full effects of these threats on species will only be felt in decades to come, yet conservation emphasizes species currently threatened with extinction, by threats that have already occurred. There have been calls for conservation to become more proactive by anticipating and protecting species that may not yet be threatened, but have a high chance of becoming threatened in the future.3,6,8,10,12,13,14 We refer to this as "over-the-horizon" extinction risk, and we identify such species among the world's nonmarine mammals by considering not only the severity of increase in threats faced by each species, but also the way each species' biology confers sensitivity or robustness to threats. We define four future risk factors based on species' biology and projected exposure to severe change in climate, human population, and land use. We regard species with two or more of these risk factors as especially vulnerable to future extinction risk.10,15,16,17,18,19 Our models predict that by 2100 up to 1,057 (20%) of nonmarine mammal species will have combinations of two or more future risk factors. These species will be particularly concentrated in two future risk hotspots in sub-Saharan Africa and southern/eastern Australia. Proactively targeting species with over-the-horizon extinction risk could help to future-proof global conservation planning and prevent a new wave of mammal species from becoming threatened with extinction by the end of this century.

Competition and geography underlie speciation and morphological evolution in Indo-Australasian monitor lizards.

How biotic and abiotic factors act together to shape biological diversity is a major question in evolutionary biology. The recent availability of large datasets and development of new methodological approaches provide new tools to evaluate the predicted effects of ecological interactions and geography on lineage diversification and phenotypic evolution. Here, we use a near complete phylogenomic-scale phylogeny and a comprehensive morphological dataset comprising more than a thousand specimens to assess the role of biotic and abiotic processes in the diversification of monitor lizards (Varanidae). This charismatic group of lizards shows striking variation in species richness among its clades and multiple instances of endemic radiation in Indo-Australasia (i.e., the Indo-Australian Archipelago and Australia), one of Earth's most biogeographically complex regions. We found heterogeneity in diversification dynamics across the family. Idiosyncratic biotic and geographic conditions appear to have driven diversification and morphological evolution in three endemic Indo-Australasian radiations. Furthermore, incumbency effects partially explain patterns in the biotic exchange between Australia and New Guinea. Our results offer insight into the dynamic history of Indo-Australasia, the evolutionary significance of competition, and the long-term consequences of incumbency effects.

Earth history events shaped the evolution of uneven biodiversity across tropical moist forests.

Far from a uniform band, the biodiversity found across Earth's tropical moist forests varies widely between the high diversity of the Neotropics and Indomalaya and the relatively lower diversity of the Afrotropics. Explanations for this variation across different regions, the "pantropical diversity disparity" (PDD), remain contentious, due to difficulty teasing apart the effects of contemporary climate and paleoenvironmental history. Here, we assess the ubiquity of the PDD in over 150,000 species of terrestrial plants and vertebrates and investigate the relationship between the present-day climate and patterns of species richness. We then investigate the consequences of paleoenvironmental dynamics on the emergence of biodiversity gradients using a spatially explicit model of diversification coupled with paleoenvironmental and plate tectonic reconstructions. Contemporary climate is insufficient in explaining the PDD; instead, a simple model of diversification and temperature niche evolution coupled with paleoaridity constraints is successful in reproducing the variation in species richness and phylogenetic diversity seen repeatedly among plant and animal taxa, suggesting a prevalent role of paleoenvironmental dynamics in combination with niche conservatism. The model indicates that high biodiversity in Neotropical and Indomalayan moist forests is driven by complex macroevolutionary dynamics associated with mountain uplift. In contrast, lower diversity in Afrotropical forests is associated with lower speciation rates and higher extinction rates driven by sustained aridification over the Cenozoic. Our analyses provide a mechanistic understanding of the emergence of uneven diversity in tropical moist forests across 110 Ma of Earth's history, highlighting the importance of deep-time paleoenvironmental legacies in determining biodiversity patterns.

Ecological interactions shape the evolution of flower color in communities across a temperate biodiversity hotspot.

Processes driving the divergence of floral traits may be integral to the extraordinary richness of flowering plants and the assembly of diverse plant communities. Several models of pollinator-mediated floral evolution have been proposed; floral divergence may (i) be directly involved in driving speciation or may occur after speciation driven by (ii) drift or local adaptation in allopatry or (iii) negative interactions between species in sympatry. Here, we generate predictions for patterns of trait divergence and community assembly expected under these three models, and test these predictions in Hakea (Proteaceae), a diverse genus in the Southwest Australian biodiversity hotspot. We quantified functional richness for two key floral traits (pistil length and flower color), as well as phylogenetic distances between species, across ecological communities, and compared these to patterns generated from null models of community assembly. We also estimated the statistical relationship between rates of trait evolution and lineage diversification across the phylogeny. Patterns of community assembly suggest that flower color, but not floral phenology or morphology, or phylogenetic relatedness, is more divergent in communities than expected. Rates of lineage diversification and flower color evolution were negatively correlated across the phylogeny and rates of flower colour evolution were positively related to branching times. These results support a role for diversity-dependent species interactions driving floral divergence during the Hakea radiation, contributing to the development of the extraordinary species richness of southwest Australia.

There is little evidence that spicy food in hot countries is an adaptation to reducing infection risk.

Spicier food in hot countries has been explained in terms of natural selection on human cultures, with spices with antimicrobial effects considered to be an adaptation to increased risk of foodborne infection. However, correlations between culture and environment are difficult to interpret, because many cultural traits are inherited together from shared ancestors, neighbouring cultures are exposed to similar conditions, and many cultural and environmental variables show strong covariation. Here, using a global dataset of 33,750 recipes from 70 cuisines containing 93 different spices, we demonstrate that variation in spice use is not explained by temperature and that spice use cannot be accounted for by diversity of cultures, plants, crops or naturally occurring spices. Patterns of spice use are not consistent with an infection-mitigation mechanism, but are part of a broader association between spice, health, and poverty. This study highlights the challenges inherent in interpreting patterns of human cultural variation in terms of evolutionary pressures.

Spatiophylogenetic modelling of extinction risk reveals evolutionary distinctiveness and brief flowering period as threats in a hotspot plant genus.

Comparative models used to predict species threat status can help identify the diagnostic features of species at risk. Such models often combine variables measured at the species level with spatial variables, causing multiple statistical challenges, including phylogenetic and spatial non-independence. We present a novel Bayesian approach for modelling threat status that simultaneously deals with both forms of non-independence and estimates their relative contribution, and we apply the approach to modelling threat status in the Australian plant genus Hakea. We find that after phylogenetic and spatial effects are accounted for, species with greater evolutionary distinctiveness and a shorter annual flowering period are more likely to be threatened. The model allows us to combine information on evolutionary history, species biology and spatial data, calculate latent extinction risk (potential for non-threatened species to become threatened), estimate the most important drivers of risk for individual species and map spatial patterns in the effects of different predictors on extinction risk. This could be of value for proactive conservation decision-making based on the early identification of species and regions of potential conservation concern.

Digest: The evolutionary relationship between environment and size in Australian rodents.

Biome shifts are thought to be relatively rare, but some clades shift among starkly different environments with relative ease. What causes these shifts, and how do they shape phenotypic evolution? Roycroft et al. found that biome shifts in the Pseudomys Division of murid rodents were repeatedly accompanied by body size evolution in accordance with Bergmann's rule, suggesting adaptive evolution in response to changing climate conditions.

Equilibrium and non-equilibrium phases in the radiation of Hakea and the drivers of diversity in Mediterranean-type ecosystems.

Mediterranean-type ecosystems (MTEs) contain exceptional plant diversity. Explanations for this diversity are usually classed as either "equilibrium," with elevated MTE diversity resulting from greater ecological carrying capacities, or "non-equilibrium," with MTEs having a greater accumulation of diversity over time than other types of ecosystems. These models have typically been considered as mutually exclusive. Here, we present a trait-based explanatory framework that incorporates both equilibrium and non-equilibrium dynamics. Using a large continental Australian plant radiation (Hakea) as a case study, we identify traits associated with niche partitioning in coexisting species (α-traits) and with environmental filtering (ß-traits), and reconstruct the mode and relative timing of diversification of these traits. Our results point to a radiation with an early non-equilibrium phase marked by divergence of ß-traits as Hakea diversified exponentially and expanded from the southwest Australian MTE into biomes across the Australian continent. This was followed from seven million years ago by an equilibrium phase, marked by diversification of α-traits and a slowdown in lineage diversification as MTE-niches became saturated. These results suggest that processes consistent with both equilibrium and non-equilibrium models have been important during different stages of the radiation of Hakea, and together they provide a richer explanation of present-day diversity patterns.

Reconstructing the Geography of Speciation from Contemporary Biodiversity Data.

Inferring the geographic mode of speciation could help reveal the evolutionary and ecological mechanisms that underlie the generation of biodiversity. Comparative methods have sought to reconstruct the geographic speciation history of clades, using data on phylogeny and species geographic ranges. However, inference from comparative methods has been limited by uncertainty over whether contemporary biodiversity data retain the historic signal of speciation. We constructed a process-based simulation model to determine the influence of speciation mode and postspeciation range evolution on current biodiversity patterns. The simulations suggest that the signal of speciation history remains detectable in species distributions and phylogeny, even when species ranges have evolved substantially through time. We extracted this signal by using a combination of summary statistics that had good power to distinguish speciation modes and then used these statistics to infer the speciation history of 30 plant and animal clades. The results point to broad taxonomic patterns in the modes of speciation, with strongest support for founder speciation in mammals and birds and strongest support for sympatric speciation in plants. Our model and analyses show that broad-scale comparative methods can be a powerful complementary approach to more focused genomic analyses in the study of the patterns and mechanisms of speciation.

Environmental niche conservatism explains the accumulation of species richness in Mediterranean-hotspot plant genera.

The causes of exceptionally high plant diversity in Mediterranean-climate biodiversity hotspots are not fully understood. We asked whether a mechanism similar to the tropical niche conservatism hypothesis could explain the diversity of four large genera (Protea, Moraea, Banksia, and Hakea) with distributions within and adjacent to the Greater Cape Floristic Region (South Africa) or the Southwest Floristic Region (Australia). Using phylogenetic and spatial data we estimated the environmental niche of each species, and reconstructed the mode and dynamics of niche evolution, and the geographic history, of each genus. For three genera, there were strong positive relationships between the diversity of clades within a region and their inferred length of occupation of that region. Within genera, there was evidence for strong evolutionary constraint on niche axes associated with climatic seasonality and aridity, with different niche optima for hotspot and nonhotspot clades. Evolutionary transitions away from hotspots were associated with increases in niche breadth and elevated rates of niche evolution. Our results point to a process of "hotspot niche conservatism" whereby the accumulation of plant diversity in Mediterranean-type ecosystems results from longer time for speciation, with dispersal away from hotspots limited by narrow and phylogenetically conserved environmental niches.

Spatial, Phylogenetic, Environmental and Biological Components of Variation in Extinction Risk: A Case Study Using Banksia.

Comparative analyses of extinction risk routinely apply methods that account for phylogenetic non-independence, but few analyses of extinction risk have addressed the possibility of spatial non-independence. We explored patterns of extinction risk in Banksia, a plant genus largely endemic to Australia's southwest biodiversity hotspot, using methods to partition the variance in two response variables (threat status and range size) into phylogenetic, spatial, and independent components. We then estimated the effects of a number of biological and external predictors on extinction risk independently of phylogeny and space. The models explained up to 34.2% of the variation in range size and up to 9.7% of the variation in threat status, nearly all of which was accounted for by the predictors, not by phylogeny or space. In the case of Banksia, therefore, high extinction risk can be clearly linked with biological syndromes (such as a brief flowering period) or geographic indicators of human impact (such as extensive habitat loss), but cannot be predicted from phylogenetic relatedness or geographic proximity.