The effects of cryptic diversity on diversification dynamics analyses in Crocodylia.

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.

Whatever criteria are used to measure evolutionary success – species numbers, geographic range, ecological abundance, ecological and life history diversity, background diversification rates, or the presence of rapidly evolving clades – the legume family is one of the most successful lineages of flowering plants. Despite this, we still know rather little about the dynamics of lineage and species diversification across the family through the Cenozoic, or about the underlying drivers of diversification. There have been few attempts to estimate net species diversification rates or underlying speciation and extinction rates for legume clades, to test whether among-lineage variation in diversification rates deviates from null expectations, or to locate species diversification rate shifts on specific branches of the legume phylogenetic tree. In this study, time-calibrated phylogenetic trees for a set of species-rich legume clades – Calliandra, Indigofereae, Lupinus, Mimosa and Robinieae – and for the legume family as a whole, are used to explore how we might approach these questions. These clades are analysed using recently developed maximum likelihood and Bayesian methods to detect species diversification rate shifts and test for among-lineage variation in speciation, extinction and net diversification rates. Possible explanations for rate shifts in terms of extrinsic factors and/or intrinsic trait evolution are discussed. In addition, several methodological issues and limitations associated with these analyses are highlighted emphasizing the potential to improve our understanding of the evolutionary dynamics of legume diversification by using much more densely sampled phylogenetic trees that integrate information across broad taxonomic, geographical and temporal levels.

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.

Phylogenies reconstructed from gene sequences can be used to investigate the tempo and mode of species diversification. Here we develop and use new statistical methods to infer past patterns of speciation and extinction from molecular phylogenies. Specifically, we test the null hypothesis that per-lineage speciation and extinction rates have remained constant through time. Rejection of this hypothesis may provide evidence for evolutionary events such as adaptive radiations or key adaptations. In contrast to previous approaches, our methods are robust to incomplete taxon sampling and are conservative with respect to extinction. Using simulation we investigate, first, the adverse effects of failing to take incomplete sampling into account and, second, the power and reliability of our tests. When applied to published phylogenies our tests suggest that, in some cases, speciation rates have decreased through time.

Amphibians constitute a diverse yet still incompletely characterized clade of vertebrates, in which new species are still being discovered and described at a high rate. Amphibians are also increasingly endangered, due in part to disease-driven threats of extinctions. As an emergency response, conservationists have begun ex situ assurance colonies for priority species. The abundance of cryptic amphibian diversity, however, may cause problems for ex situ conservation. In this study we used a DNA barcoding approach to survey mitochondrial DNA (mtDNA) variation in captive populations of 10 species of Neotropical amphibians maintained in an ex situ assurance programme at El Valle Amphibian Conservation Center (EVACC) in the Republic of Panama. We combined these mtDNA sequences with genetic data from presumably conspecific wild populations sampled from across Panama, and applied genetic distance-based and character-based analyses to identify cryptic lineages. We found that three of ten species harboured substantial cryptic genetic diversity within EVACC, and an additional three species harboured cryptic diversity among wild populations, but not in captivity. Ex situ conservation efforts focused on amphibians are therefore vulnerable to an incomplete taxonomy leading to misidentification among cryptic species. DNA barcoding may therefore provide a simple, standardized protocol to identify cryptic diversity readily applicable to any amphibian community.

BackgroundTranscriptome sequencing has become a method of choice for evolutionary studies in microbial eukaryotes due to low cost and minimal sample requirements. Transcriptome data has been extensively used in phylogenomic studies to infer ancient evolutionary histories. However, its utility in studying cryptic species diversity is not well explored. An empirical investigation was conducted to test the applicability of transcriptome data in resolving two major types of discordances at lower taxonomic levels. These include cases where species have the same morphology but different genetics (cryptic species) and species of different morphologies but have the same genetics. We built a species comparison bioinformatic pipeline that takes into account the nature of transcriptome data in amoeboid microbes exemplifying such discordances.ResultOur analyses of known or suspected cryptic species yielded consistent results regardless of the methods of culturing, RNA collection or sequencing. Over 95% of the single copy genes analyzed in samples of the same species sequenced using different methods and cryptic species had intra- and interspecific divergences below 2%. Only a minority of groups (2.91–4.87%) had high distances exceeding 2% in these taxa, which was likely caused by low data quality. This pattern was also observed in suspected genetically similar species with different morphologies. Transcriptome data consistently delineated all taxa above species level, including cryptically diverse species. Using our approach we were able to resolve cryptic species problems, uncover misidentification and discover new species. We also identified several potential barcode markers with varying evolutionary rates that can be used in lineages with different evolutionary histories.ConclusionOur findings demonstrate that transcriptome data is appropriate for understanding cryptic species diversity in microbial eukaryotes.

A long‐standing question in evolutionary biology is how historical biogeographic processes have shaped the current diversity of organisms, especially for highly diverse groups. We study the diversification dynamics and biogeographic processes of one of the most diverse families of Lepidoptera, Geometridae, with over 24,000 described species and a worldwide distribution. Despite the cosmopolitan distribution of the family, most species of Geometridae have limited distribution ranges. We present the largest historical biogeography and diversification study on the current diversity patterns and distribution ranges of Geometridae. We use a multi‐locus dataset of 1200 taxa to estimate the historical biogeography of Geometridae, implementing a Bayesian approach of the Dispersal‐Extinction‐Cladogenesis (DEC) model that incorporates palaeographic‐based dispersal graphs with uncertainty in geological ages in RevBayes. We also implement a Bayesian time‐variable, episodic birth–death model and a model that allows branch‐specific speciation rates to estimate the diversification dynamics in the family. Our results suggest that the most recent common ancestor of Geometridae was distributed in the New World, with the Neotropics being the most likely ancestral area. An increase in diversification rates occurred circa 30–40 million years ago (Mya), coinciding with a time of a major global climate cooling in the Eocene. Clade‐specific shifts in speciation rates also occurred around 10–15 Mya, coincident with another period of major climate change in the Oligocene. Our results point to different biogeographical and evolutionary histories per area to show the differences of the diversification rates in different biogeographical regions through time, showing the relative importance of each region in the diversification history of Geometridae.

Historical biogeography of North American killifishes (Cyprinodontiformes) recapitulates geographical history in the Gulf of México watershed

Freshwater ecosystems represent hotspots for the world’s total diversity and human well-being. However, they are also subjected to threats across the globe as a result of localised human activities, broad scale catchment clearance, climate change and invasive species. The increased degradation of freshwater habitats and their ecological functions as a consequence of these threats, at local and global scales, has led to significant freshwater problems for human existence and the world’s biodiversity. There is growing evidence that the loss of biodiversity is one of the most complex environmental issues facing the world; however, the importance of understanding species distribution patterns and the ecological differentiation among species that are reflected as species-specific responses or tolerances to environmental drivers is less well understood. In particular, when a morphological approach is used as a taxonomic tool for investigating species diversity and species level responses to environmental drivers, the diversity of responses hidden within species complexes may not be realized, and the conclusion of generality may mask specific cryptic species responses. In South-East Queensland, Australia, European occupation since the mid 1800’s has seen large scale clearing of native vegetation along streams and rivers in nearly all catchments. As a consequence of this land-use change catchment hydrology has been substantially altered, which, combined with the presence of dams and weirs, has resulted in a decline in water quality of streams in some catchments, which is of growing concern for conservation of species biodiversity. This study aimed to explore cryptic diversity in two species complexes of freshwater aytid shrimps common in South-East Queensland and elucidate species level responses to environmental variation that could explain their spatial distribution. This broad aim was met through three specific studies. First, using regional scale data of cryptic species diversity and water quality, the importance of species-specific responses to environmental conditions in determining spatial distribution patterns and environmental relationships of cryptic species in the Caridina indistincta and Paratya australiensis species complexes was examined. To accomplish this aim, DNA sequences were used to identify shrimp specimens from 89 sites in 17 catchments spanning the study area. In addition, an assessment of eight morphological traits was used to test whether these cryptic species could be morphologically identified. Use of these eight traits did allow species level identification, at least in South-East Queensland. However, caution is suggested in the use of these morphological traits for recognising species, due to the probability of morphological plasticity within a species across broad spatial scales. Ordination analysis of presence-absence data showed that the five cryptic species within the two species complexes showed spatially distinct distributions across streams in SEQ, with each cryptic species displaying different relationships with individual environmental variables. For species in the Caridina indistincta complex, C. indistincta sp. B was significantly associated with elevation, C. indistincta sp. D was significantly correlated with dissolved oxygen range, whilst, individuals of C. indistincta sp. A were negatively associated with elevation and dissolved oxygen range. This may indicate that C. indistincta sp. A tended to inhabit sites with low elevation and perhaps having a higher tolerance to a low range of dissolved oxygen. For the Paratya australiensis species complex, P. australiensis lineage 4 and 6 showed significant correlations with elevation and conductivity, respectively. The second broad aim of the study was to explore these spatial patterns at smaller geographical scales and with greater detail about water quality to understand and quantify the fundamental environmental factors (e.g., physical chemical water parameters and concentrations of heavy metals) that are potentially shaping the current distribution patterns and abundance of cryptic species within the two species complexes. To explore this aim, sediment samples from 22 sites in 13 catchments in SEQ were analysed to determine concentrations (mg/kg dry weight) of 11 heavy metals. Additionally, a number of water quality variables were measured in situ, including: elevation, stream width, stream temperature, dissolved oxygen, conductivity, pH, total dissolved solids, and turbidity. Also, a water sample was taken from each site for laboratory analysis of: Ammonium nitrogen (NH4-N), Dissolved oxidized nitrogen (Nitrate+Nitrite) (NOX-N), Total nitrogen (TN), Total kjeldahl nitrogen (TKN), Total kjeldahl phosphorus (TKP), Orthophosphate-P (PO4-P). Shrimps were collected from each site and identified to species using both morphology and DNA sequencing. The morphological identification of each adult individual (except juveniles which were genetically analysed) was used as a measure of absolute abundance and the genetic ‘checking’ of a set number of individuals in each sample was used to compute relative abundance. Redundancy analysis (RDA) showed that the spatial distribution and absolute and relative abundance of C. indistincta sp. D and sp. B were significantly positively influenced by elevation, while the relative abundance of P. australiensis Lin.6 was significantly positively affected by the concentration of manganese (Mn). Stream Total nitrogen (TN) was significantly positive driver of the spatial distribution and relative abundance of C. indistincta sp. A, while Orthophosphate-P (PO4-P) was significantly positive driver for the absolute and relative abundance of this species. Further analysis, this study confirms that P. australiensis Lin.6 was more tolerant of heavy metal concentrations compared with other cryptic species, as its distribution and absolute and relative abundance were significantly positively correlated with the concentrations of manganese, iron and cobalt. In contrast, C. indistincta sp. A was more sensitive to these metals than other study species. These results demonstrated that cryptic species of freshwater atyid shrimps of the C. indistincta and P. australiensis species complexes were different in their environmental requirements. As well, the cryptic species of both complexes were identified to have different associations with heavy metal concentrations, indicating that these species were different in their tolerance to toxicants. Finally, the third aim of the study was to further examine the differences in sensitivity to heavy metals (Copper and Zinc) among cryptic species of the two study complexes experimentally in the laboratory. Two cryptic species of each complex were used as study species, C. indistincta sp. A and sp. D and P. australiensis Lin.4 and Lin.6. The field studies showed differences among these species in their correlations with metal concentrations, and therefore they were seen as good candidate species for testing differences in the sensitivity to metal toxicants. Each cryptic species was exposed to six concentrations of each metal Cu or Zn using an acute (96-h) toxicity test. The results from this study were generally showed contrasting correlation between species and heavy metals; P. australiensis Lin.6 was the most tolerant species to both study metals, while C. indistincta sp. A was more sensitive to copper, and C. indistincta sp. D was more sensitive to Zn compared with the other tested species. Furthermore, the exposure of individuals of each species to the heavy metals caused changes in both their behaviour and their colour during exposure time. Overall, this study has shown cryptic species within broad species complexes can vary in their spatial distribution and their tolerance and response to water quality parameters. This highlights the advantage of using analyses of biotic and abiotic variables for ecological management and biodiversity conservation and the need to understand true species diversity when looking at species level responses to environmental degradation.

BackgroundCryptic species are two or more distinct but morphologically similar species that were classified as a single species. During the past two decades we observed an exponential growth of publications on cryptic species. Recently published reviews have demonstrated cryptic species have profound consequences on many biological disciplines. It has been proposed that their distribution is non-random across taxa and biomes.ResultsWe analysed a literature database for the taxonomic and biogeographical distribution of cryptic animal species reports. Results from regression analysis indicate that cryptic species are almost evenly distributed among major metazoan taxa and biogeographical regions when corrected for species richness and study intensity.ConclusionThis indicates that morphological stasis represents an evolutionary constant and that cryptic metazoan diversity does predictably affect estimates of earth's animal diversity. Our findings have direct theoretical and practical consequences for a number of prevailing biological questions with regard to global biodiversity estimates, conservation efforts and global taxonomic initiatives.

The temporal dynamics of evolutionary diversification in Ipomoea

BackgroundDiet is a key component of a species ecological niche and plays critical roles in guiding the trajectories of evolutionary change. Previous studies suggest that dietary evolution can influence the rates and patterns of species diversification, with omnivorous (animal and plant, ‘generalist’) diets slowing down diversification compared to more restricted (‘specialist’) herbivorous and carnivorous diets. This hypothesis, here termed the “dietary macroevolutionary sink” hypothesis (DMS), predicts that transitions to omnivorous diets occur at higher rates than into any specialist diet, and omnivores are expected to have the lowest diversification rates, causing an evolutionary sink into a single type of diet. However, evidence for the DMS hypothesis remains conflicting. Here, we present the first test of the DMS hypothesis in a lineage of ectothermic tetrapods—the prolific Liolaemidae lizard radiation from South America.ResultsAncestral reconstructions suggest that the stem ancestor was probably insectivorous. The best supported trait model is a diet-dependent speciation rate, with independent extinction rates. Herbivory has the highest net diversification rate, omnivory ranks second, and insectivory has the lowest. The extinction rate is the same for all three diet types and is much lower than the speciation rates. The highest transition rate was from omnivory to insectivory, and the lowest transition rates were between insectivory and herbivory.ConclusionsOur findings challenge the core prediction of the DMS hypothesis that generalist diets represent an ‘evolutionary sink’. Interestingly, liolaemid lizards have rapidly and successfully proliferated across some of the world’s coldest climates (at high elevations and latitudes), where species have evolved mixed arthropod-plant (omnivore) or predominantly herbivore diets. This longstanding observation is consistent with the higher net diversification rates found in both herbivory and omnivory. Collectively, just like the evolution of viviparity has been regarded as a ‘key adaptation’ during the liolaemid radiation across cold climates, our findings suggest that transitions from insectivory to herbivory (bridged by omnivory) are likely to have played a role as an additional key adaptation underlying the exceptional diversification of these reptiles across extreme climates.

Analysing diversification dynamics is key to understanding the past evolutionary history of clades that led to present‐day biodiversity patterns. While such analyses are widespread in well‐characterized groups of species, they are much more challenging in groups for which diversity is mostly known through molecular techniques. Here, we use the largest global database on the small subunit (SSU) rRNA gene of Glomeromycotina, a subphylum of microscopic arbuscular mycorrhizal fungi that provide mineral nutrients to most land plants by forming one of the oldest terrestrial symbioses, to analyse the diversification dynamics of this clade in the past 500 million years. We perform a range of sensitivity analyses and simulations to control for potential biases linked to the nature of the data. We find that Glomeromycotina tend to have low speciation rates compared to other eukaryotes. After a peak of speciations between 200 and 100 million years ago, they experienced an important decline in speciation rates toward the present. Such a decline could be at least partially related to a shrinking of their mycorrhizal niches and to their limited ability to colonize new niches. Our analyses identify patterns of diversification in a group of obligate symbionts of major ecological and evolutionary importance and illustrate that short molecular markers combined with intensive sensitivity analyses can be useful for studying diversification dynamics in microbial groups.

Amazonia is extremely biodiverse, but the mechanisms for the origin of this diversity are still under debate. We propose a diversification model for Amazonia based on the interplay of intrinsic clade functional traits, habitat associations and past geological events, using as a model group the species-rich Neotropical family Marantaceae. Our results show that the species richness of the lineage is predicted by functional strategy, rather than clade age, and thus the fast vs. slow growth functional trade-off is a major determinant of clade diversification in Marantaceae. Rapidly growing clades were mostly associated with highly productive habitats, and their origin and diversification dynamics matched the expansion of fertile soils mediated by Andean uplift c. 23 Mya. Fast-growth strategies probably led to fast molecular evolution, speeding up speciation rates and species accumulation, resulting in higher numbers of extant species. Our results indicate that pure allopatric-dispersal models disconnected from past geological and ecological forces may be inadequate for explaining the evolutionary and diversity patterns in Amazonian lowlands. We suggest that a coupling of the functional trait-niche framework with diversification dynamics provides insights into the evolutionary history of tropical forests and helps elucidate the mechanisms underlying the origin and evolution of its spectacular biodiversity.

Lineages arriving on islands may undergo explosive evolutionary radiations owing to the wealth of ecological opportunities. Although studies on insular taxa have improved our understanding of macroevolutionary phenomena, we know little about the macroevolutionary dynamics of continental exchanges. Here we study the evolution of eight Carnivora families that have migrated across the Northern Hemisphere to investigate if continental invasions also result in explosive diversification dynamics. We used a Bayesian approach to estimate speciation and extinction rates from a substantial dataset of fossil occurrences while accounting for the incompleteness of the fossil record. Our analyses revealed a strongly asymmetrical pattern in which North American lineages invading Eurasia underwent explosive radiations, whereas lineages invading North America maintained uniform diversification dynamics. These invasions into Eurasia were characterized by high rates of speciation and extinction. The radiation of the arriving lineages in Eurasia coincide with the decline of established lineages or phases of climate change, suggesting differences in the ecological settings between the continents may be responsible for the disparity in diversification dynamics. These results reveal long-term outcomes of biological invasions and show that the importance of explosive radiations in shaping diversity extends beyond insular systems and have significant impact at continental scales.