Why Do Some Lineages Radiate While Others Do Not? Perspectives for Future Research on Adaptive Radiations.

Understanding the processes that drive phenotypic diversification and underpin speciation is key to elucidating how biodiversity has evolved. Although these processes have been studied across a wide array of clades, adaptive radiations (ARs), which are systems with multiple closely related species and broad phenotypic diversity, have been particularly fruitful for teasing apart the factors that drive and constrain diversification. As such, ARs have become popular candidate study systems for determining the extent to which ecological features, including aspects of organisms and the environment, and inter- and intraspecific interactions, led to evolutionary diversification. Despite substantial past empirical and theoretical work, understanding mechanistically how ARs evolve remains a major challenge. Here, we highlight a number of understudied components of the environment and of lineages themselves, which may help further our understanding of speciation and AR. We also outline some substantial remaining challenges to achieving a detailed understanding of adaptation, speciation, and the role of ecology in these processes. These major challenges include identifying factors that have a causative impact in promoting or constraining ARs, gaining a more holistic understanding of features of organisms and their environment that interact resulting in adaptation and speciation, and understanding whether the role of these organismal and environmental features varies throughout the radiation process. We conclude by providing perspectives on how future investigations into the AR process can overcome these challenges, allowing us to glean mechanistic insights into adaptation and speciation.

The Role of Hybridization in Species Formation and Persistence.

Hybridization, or interbreeding between different taxa, was traditionally considered to be rare and to have a largely detrimental impact on biodiversity, sometimes leading to the breakdown of reproductive isolation and even to the reversal of speciation. However, modern genomic and analytical methods have shown that hybridization is common in some of the most diverse clades across the tree of life, sometimes leading to rapid increase of phenotypic variability, to introgression of adaptive alleles, to the formation of hybrid species, and even to entire species radiations. In this review, we identify consensus among diverse research programs to show how the field has progressed. Hybridization is a multifaceted evolutionary process that can strongly influence species formation and facilitate adaptation and persistence of species in a rapidly changing world. Progress on testing this hypothesis will require cooperation among different subdisciplines.

Hybridization and Transgressive Evolution Generate Diversity in an Adaptive Radiation of Anolis Lizards.

Interspecific hybridization may act as a major force contributing to the evolution of biodiversity. Although generally thought to reduce or constrain divergence between 2 species, hybridization can, paradoxically, promote divergence by increasing genetic variation or providing novel combinations of alleles that selection can act upon to move lineages toward new adaptive peaks. Hybridization may, then, play a key role in adaptive radiation by allowing lineages to diversify into new ecological space. Here, we test for signatures of historical hybridization in the Anolis lizards of Puerto Rico and evaluate 2 hypotheses for the role of hybridization in facilitating adaptive radiation-the hybrid swarm origins hypothesis and the syngameon hypothesis. Using whole genome sequences from all 10 species of Puerto Rican anoles, we calculated D and f-statistics (from ABBA-BABA tests) to test for introgression across the radiation and employed multispecies network coalescent methods to reconstruct phylogenetic networks that allow for hybridization. We then analyzed morphological data for these species to test for patterns consistent with transgressive evolution, a phenomenon in which the trait of a hybrid lineage is found outside of the range of its 2 parents. Our analyses uncovered strong evidence for introgression at multiple stages of the radiation, including support for an ancient hybrid origin of a clade comprising half of the extant Puerto Rican anole species. Moreover, we detected significant signals of transgressive evolution for 2 ecologically important traits, head length and toepad width, the latter of which has been described as a key innovation in Anolis. [Adaptive radiation; introgression; multispecies network coalescent; phenotypic evolution; phylogenetic network; reticulation; syngameon; transgressive segregation.].

Female dewlap ornaments are evolutionarily labile and associated with increased diversification rates in Anolis lizards.

The evolution of costly signalling traits has largely focused on male ornaments. However, our understanding of ornament evolution is necessarily incomplete without investigating the causes and consequences of variation in female ornamentation. Here, we study the Anolis lizard dewlap, a trait extensively studied as a male secondary sexual characteristic but present in females of several species. We characterized female dewlaps for 339 species to test hypotheses about their evolution. Our results did not support the hypothesis that female dewlaps are selected against throughout the anole phylogeny. Rather, we found that female dewlaps were evolutionary labile. We also did not find support for the adaptive hypothesis that interspecific competition drove the evolution of female dewlaps. However, we did find support for the pleiotropy hypothesis as species with larger females and reduced sexual size dimorphism were more likely to possess female dewlaps. Lastly, we found that female dewlap presence influenced diversification rates in anoles, but only secondarily to a hidden state. Our results demonstrate that female ornamentation is widespread in anoles and the traditional hypothesis of divergent selection between the sexes does not fully explain their evolution. Instead, female ornamentation is likely to be subject to complex adaptive and non-adaptive evolutionary forces.

Phenotypic and genomic diversification with isolation by environment along elevational gradients in a neotropical treefrog.

Understanding how geographic and environmental heterogeneity drive local patterns of genetic variation is a major goal of ecological genomics and a key question in evolutionary biology. The tropical Andes and inter-Andean valleys are shaped by markedly heterogeneous landscapes, where species experience strong selective processes. We examined genome-wide SNP data together with behavioural and ecological traits (mating calls and body size) known to contribute to genetic isolation in anurans in the banana tree-dwelling frog, Boana platanera, distributed across an environmental gradient in Central Colombia (northern South America). Here, we analysed the relationships between environmentally (temperature and precipitation) associated genetic and phenotypic differentiation and the potential drivers of isolation by environment along an elevation gradient. We identified candidate SNPs associated with temperature and body size, which follow a clinal pattern of genome-wide differentiation tightly coupled with phenotypic variation: as elevation increases, B. platanera exhibits larger body size and longer call duration with more pulses but lower pulse rate and frequency. Thus, the environmental landscape has rendered a scenario where isolation by environment and candidate loci show concordance with phenotypic divergence in this tropical frog along an elevation gradient in the Colombian Andes. Our study sets the basis for evaluating the role of temperature in the genetic structure and local adaptation in tropical treefrogs and its putative effect on life cycle (embryos, tadpoles, adults) along elevation gradients.

Biome stability predicts population structure of a southern African aridland bird species.

Environments are heterogeneous in space and time, and the permeability of landscape and climatic barriers to gene flow may change over time. When barriers are present, they may start populations down the path toward speciation, but if they become permeable before the process of speciation is complete, populations may once more merge. In Southern Africa, aridland biomes play a central role in structuring the organization of biodiversity. These biomes were subject to substantial restructuring during Plio-Pleistocene climatic fluctuations, and the imprint of this changing environment should leave genetic signatures on the species living there. Here, we investigate the role of adjacent aridland biome boundaries in structuring the genetic diversity within a widespread generalist bird, the Cape Robin-chat (Cossypha caffra). We find evidence supporting a central role for aridland biomes in structuring populations across Southern Africa. Our findings support a scenario wherein populations were isolated in different biome refugia, due to separation by the exceptionally arid Nama Karoo biome. This biome barrier may have arisen through a combination of habitat instability and environmental unsuitability, and was highly unstable throughout the Plio-Pleistocene. However, we also recovered a pattern of extensive contemporary gene flow and admixture across the Nama Karoo, potentially driven by the establishment of homesteads over the past 200 years. Thus, the barrier has become permeable, and populations are currently merging. This represents an instance where initial formation of a barrier to gene flow enabled population differentiation, with subsequent gene flow and the merging of populations after the barrier became permeable.

Comparing Adaptive Radiations Across Space, Time, and Taxa.

Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.

Genome-wide epigenetic isolation by environment in a widespread Anolis lizard.

Epigenetic changes can provide a pathway for organisms to respond to local environmental conditions by influencing gene expression. However, we still know little about the spatial distribution of epigenetic variation in natural systems, how it relates to the distribution of genetic variation and the environmental structure of the landscape, and the processes that generate and maintain it. Studies examining spatial patterns of genetic and epigenetic variation can provide valuable insights into how ecological and population processes contribute to epigenetic divergence across heterogeneous landscapes. Here, we perform a comparative analysis of spatial genetic and epigenetic variation based on 8,459 single nucleotide polymorphisms (SNPs) and 8,580 single methylation variants (SMVs) from eight populations of the Puerto Rican crested anole, Anolis cristatellus, an abundant lizard in the adaptive radiations of anoles on the Greater Antilles that occupies a diverse range of habitats. Using generalized dissimilarity modelling and multiple matrix regression, we found that genome-wide epigenetic differentiation is strongly correlated with environmental divergence, even after controlling for the underlying genetic structure. We also detected significant associations between key environmental variables and 96 SMVs, including 42 located in promoter regions or gene bodies. Our results suggest an environmental basis for population-level epigenetic differentiation in this system and contribute to better understanding how environmental gradients structure epigenetic variation in nature.

Squeezing water from a stone: high-throughput sequencing from a 145-year old holotype resolves (barely) a cryptic species problem in flying lizards.

We used Massively Parallel High-Throughput Sequencing to obtain genetic data from a 145-year old holotype specimen of the flying lizard, Draco cristatellus. Obtaining genetic data from this holotype was necessary to resolve an otherwise intractable taxonomic problem involving the status of this species relative to closely related sympatric Draco species that cannot otherwise be distinguished from one another on the basis of museum specimens. Initial analyses suggested that the DNA present in the holotype sample was so degraded as to be unusable for sequencing. However, we used a specialized extraction procedure developed for highly degraded ancient DNA samples and MiSeq shotgun sequencing to obtain just enough low-coverage mitochondrial DNA (721 base pairs) to conclusively resolve the species status of the holotype as well as a second known specimen of this species. The holotype was prepared before the advent of formalin-fixation and therefore was most likely originally fixed with ethanol and never exposed to formalin. Whereas conventional wisdom suggests that formalin-fixed samples should be the most challenging for DNA sequencing, we propose that evaporation during long-term alcohol storage and consequent water-exposure may subject older ethanol-fixed museum specimens to hydrolytic damage. If so, this may pose an even greater challenge for sequencing efforts involving historical samples.

Toxic toad invasion of Wallacea: A biodiversity hotspot characterized by extraordinary endemism.

(a) A map of Wallacea showing islands invaded by Duttaphrynus melanostictus in red, islands inhabited by Varanus komodoensis in blue, and localities of genetic samples in yellow points. (b) A D. melanostictus from Lombok Island. (c) Environmental niche model for the Sunda Islands clade of D. melanostictus projected into Wallacea. Green color indicates very high suitability, yellow color indicates high suitability, and orange color indicates moderate suitability.

Life History Traits and Niche Instability Impact Accuracy and Temporal Transferability for Historically Calibrated Distribution Models of North American Birds.

A primary assumption of environmental niche models (ENMs) is that models are both accurate and transferable across geography or time; however, recent work has shown that models may be accurate but not highly transferable. While some of this is due to modeling technique, individual species ecologies may also underlie this phenomenon. Life history traits certainly influence the accuracy of predictive ENMs, but their impact on model transferability is less understood. This study investigated how life history traits influence the predictive accuracy and transferability of ENMs using historically calibrated models for birds. In this study I used historical occurrence and climate data (1950-1990s) to build models for a sample of birds, and then projected them forward to the 'future' (1960-1990s). The models were then validated against models generated from occurrence data at that 'future' time. Internal and external validation metrics, as well as metrics assessing transferability, and Generalized Linear Models were used to identify life history traits that were significant predictors of accuracy and transferability. This study found that the predictive ability of ENMs differs with regard to life history characteristics such as range, migration, and habitat, and that the rarity versus commonness of a species affects the predicted stability and overlap and hence the transferability of projected models. Projected ENMs with both high accuracy and transferability scores, still sometimes suffered from over- or under- predicted species ranges. Life history traits certainly influenced the accuracy of predictive ENMs for birds, but while aspects of geographic range impact model transferability, the mechanisms underlying this are less understood.

Natural history collections as windows on evolutionary processes.

Natural history collections provide an immense record of biodiversity on Earth. These repositories have traditionally been used to address fundamental questions in biogeography, systematics and conservation. However, they also hold the potential for studying evolution directly. While some of the best direct observations of evolution have come from long-term field studies or from experimental studies in the laboratory, natural history collections are providing new insights into evolutionary change in natural populations. By comparing phenotypic and genotypic changes in populations through time, natural history collections provide a window into evolutionary processes. Recent studies utilizing this approach have revealed some dramatic instances of phenotypic change over short timescales in response to presumably strong selective pressures. In some instances, evolutionary change can be paired with environmental change, providing a context for potential selective forces. Moreover, in a few cases, the genetic basis of phenotypic change is well understood, allowing for insight into adaptive change at multiple levels. These kinds of studies open the door to a wide range of previously intractable questions by enabling the study of evolution through time, analogous to experimental studies in the laboratory, but amenable to a diversity of species over longer timescales in natural populations.

Deep genetic structure and ecological divergence in a widespread human commensal toad.

The Asian common toad (Duttaphrynus melanostictus) is a human commensal species that occupies a wide variety of habitats across tropical Southeast Asia. We test the hypothesis that genetic variation in D. melanostictus is weakly associated with geography owing to natural and human-mediated dispersal facilitated by its commensal nature. Phylogenetic and population genetic analyses of mitochondrial and nuclear DNA sequence variation, and predictive species distribution modelling, unexpectedly recovered three distinct evolutionary lineages that differ genetically and ecologically, corresponding to the Asian mainland, coastal Myanmar and the Sundaic islands. The persistence of these three divergent lineages, despite ample opportunities for recent human-mediated and geological dispersal, suggests that D. melanostictus actually consists of multiple species, each having narrower geographical ranges and ecological niches, and higher conservation value, than is currently recognized. These findings also have implications for the invasion potential of this human commensal elsewhere, such as in its recently introduced ranges on the islands of Borneo, Sulawesi, Seram and Madagascar.

Niche divergence builds the case for ecological speciation in skinks of the Plestiodon skiltonianus species complex.

Adaptation to different thermal environments has the potential to cause evolutionary changes that are sufficient to drive ecological speciation. Here, we examine whether climate-based niche divergence in lizards of the Plestiodon skiltonianus species complex is consistent with the outcomes of such a process. Previous work on this group shows that a mechanical sexual barrier has evolved between species that differ mainly in body size and that the barrier may be a by-product of selection for increased body size in lineages that have invaded xeric environments; however, baseline information on niche divergence among members of the group is lacking. We quantified the climatic niche using mechanistic physiological and correlative niche models and then estimated niche differences among species using ordination techniques and tests of niche overlap and equivalency. Our results show that the thermal niches of size-divergent, reproductively isolated morphospecies are significantly differentiated and that precipitation may have been as important as temperature in causing increased shifts in body size in xeric habitats. While these findings alone do not demonstrate thermal adaptation or identify the cause of speciation, their integration with earlier genetic and behavioral studies provides a useful test of phenotype-environment associations that further support the case for ecological speciation in these lizards.

Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians.

Population declines and extinctions of amphibians have been attributed to the chytrid fungus Batrachochytrium dendrobatidis (Bd), especially one globally emerging recombinant lineage ('Bd-GPL'). We used PCR assays that target the ribosomal internal transcribed spacer region (ITS) of Bd to determine the prevalence and genetic diversity of Bd in South Korea, where Bd is widely distributed but is not known to cause morbidity or mortality in wild populations. We isolated Korean Bd strains from native amphibians with low infection loads and compared them to known worldwide Bd strains using 19 polymorphic SNP and microsatellite loci. Bd prevalence ranged between 12.5 and 48.0%, in 11 of 17 native Korean species, and 24.7% in the introduced bullfrog Lithobates catesbeianus. Based on ITS sequence variation, 47 of the 50 identified Korean haplotypes formed a group closely associated with a native Brazilian Bd lineage, separated from the Bd-GPL lineage. However, multilocus genotyping of three Korean Bd isolates revealed strong divergence from both Bd-GPL and the native Brazilian Bd lineages. Thus, the ITS region resolves genotypes that diverge from Bd-GPL but otherwise generates ambiguous phylogenies. Our results point to the presence of highly diversified endemic strains of Bd across Asian amphibian species. The rarity of Bd-GPL-associated haplotypes suggests that either this lineage was introduced into Korea only recently or Bd-GPL has been outcompeted by native Bd strains. Our results highlight the need to consider possible complex interactions among native Bd lineages, Bd-GPL and their associated amphibian hosts when assessing the spread and impact of Bd-GPL on worldwide amphibian populations.

Has the Earth's sixth mass extinction already arrived?

Palaeontologists characterize mass extinctions as times when the Earth loses more than three-quarters of its species in a geologically short interval, as has happened only five times in the past 540 million years or so. Biologists now suggest that a sixth mass extinction may be under way, given the known species losses over the past few centuries and millennia. Here we review how differences between fossil and modern data and the addition of recently available palaeontological information influence our understanding of the current extinction crisis. Our results confirm that current extinction rates are higher than would be expected from the fossil record, highlighting the need for effective conservation measures.