The phylogenetic limits to diversity-dependent diversification

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence their diversification? In other words: are there phylogenetic limits to this diversity-dependence? Islands form ideal systems to answer these questions, because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, i.e. all mainland species can colonize and diversify independently from one another. We term this clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all island species of a taxonomic group regardless of their mainland ancestry, i.e. diversity-dependence applies both to species within the same clade and between different clades established by different mainland species. We call this island-wide (IW) diversity-dependence. We present a method to compute a likelihood for this model given phylogenetic data on colonization and branching events and use likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes which are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e. IW diversity-dependence. But it could also be suggestive of only within-clade interactions, because between-clade interactions would have blocked the same ecotype re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations, while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to diversity-dependent diversification. We discuss possibilities for future extensions and applications of our modelling approach.</p

The limits to ecological limits to diversification

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification, i.e., ecological limits to diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence their diversification? In other words: are there phylogenetic limits to these ecological limits? Islands form ideal systems to answer these questions, because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, which we term clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all species regardless of their ancestry, i.e. diversity-dependence applies both to species within the same clade and between different clades. We call this island-wide (IW) diversity-dependence. Here we present a method to compute a likelihood for this model and develop a statistical procedure based on likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes which are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e. IW diversity-dependence. But it could also be suggestive of only within-clade interactions, because between-clade interactions would have blocked the same ecotype re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations, while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to ecological limits to diversification. We discuss how our new IW model advances our understanding also in other ways, ranging from identifying priority effects to modelling the spread of an epidemic in island-like systems, such as schools or hospitals

Patrones de abundancia de la macrofauna asociada a macroalgas marinas a largo de la Península Ibérica

macroalgae were studied on a spatial scale along the Iberian Peninsula. Nineteen stations and four dominant algae were selected (intertidal zone: Corallina elongata and Asparagopsis armata; subtidal zone: Stypocaulon scoparium and Cladostephus spongiosus). Five environmental factors were also considered (seawater temperature, conductivity, dissolved oxygen, turbidity and pH). The Atlantic coast was characterized by lower temperature and conductivity as well as higher values of oxygen and turbidity than the Mediterranean coast. A total of 106274 macrofaunal specimens were sorted and examined (68% arthropods, 27% molluscs, 4% annelids and 1% echinoderms). Crustaceans were the dominant group in all the macroalgae (ca. 80% in C. elongata and A. armata, ca. 50% in S. scoparium and C. spongiosus) followed by molluscs, which were more abundant in the subtidal algae (ca. 40%) than in intertidal ones (ca.10%). Abundance patterns of macrofauna along the Iberian Peninsula were similar in the four studied algae. Most of crustaceans belonged to the order Amphipoda, which showed high densities (>1000 ind/1000 ml algae) along the whole Peninsula; isopods showed the highest abundances in the Atlantic, while tanaids, cumaceans and decapods were more abundant in the Mediterranean. Among molluscs, gasteropods showed highest abundances along the Atlantic coasts, whereas bivalves showed higher densities along the MediterraneanSe llevó a cabo un estudio espacial de los patrones de abundancia y distribución de la macrofauna asociada a macroalgas a lo largo de la Península Ibérica. Se seleccionaron 19 estaciones y 4 algas dominantes (zona intermareal: Corallina elongata y Asparagopsis armata; zona submareal: Stypocaulon scoparium y Cladostephus spongiosus). Se consideraron también cinco variables ambientales (temperatura del agua, conductividad, oxígeno disuelto, turbidez y pH). La costa atlántica se caracterizó por valores más bajos de temperatura y conductividad, y más altos de oxígeno y turbidez. Se examinaron 106274 individuos de la macrofauna (68% artrópodos, 27% moluscos, 4% anélidos y 1% equinodermos). Los crustáceos fueron dominantes en todas las macroalgas (alrededor del 80% en C. elongata y A. armata, y en torno al 50% en S. scoparium y C. spongiosus), seguidos por los moluscos, que fueron más abundantes en el submareal (40%) que en el intermareal (10%). Los patrones de abundancia de la macrofauna a lo largo de la Península Ibérica fueron similares en las cuatro algas estudiadas. La mayoría de los crustáceos pertenecieron al orden Amphipoda, que mostró densidades muy altas (>1000 ind/1000 ml alga) en toda la Península; los isópodos mostraron las mayores densidades en el Atlántico, mientras que los tanaidáceos, cumáceos y decápodos fueron más abundantes en el Mediterráneo. Entre los moluscos, los gasterópodos mostraron abundancias mayores en el Atlántico, mientras que los bivalvos dominaron en el Mediterráneo. Teniendo en cuenta que todas las estaciones seleccionadas no tenían influencia antrópica importante, los patrones de abundancia obtenidos podrían explicarse en base a diferencias naturales en la temperatura del agua, oxígeno, conductividad y turbidez, existiendo un gradiente transicional entre taxones de aguas más cálidas (del norte de Africa y del Mediterráneo) y taxones de aguas más frías (del Mar del Norte y el Ártico)

Patrones de diversificación en anfibios neotropicales

La Tierra alberga una extraordinaria diversidad entre sus formas de vidas a todos sus niveles, genética, específica o ecosistémica. Dicha diversidad no se distribuye de manera equilibrada, encontrándose grandes diferencias entre grupos de organismos y distintas regiones del planeta. Pero, ¿por qué determinados clados y/o regiones albergan una mayor biodiversidad? Esta es una cuestión de gran complejidad, que ha intrigado durante décadas a los investigadores y cuya respuesta implica comprender cómo se origina la biodiversidad en diferentes niveles. Desde los proceso de especiación, extinción y dispersión que explican los patrones a gran escala, y el conjunto de factores que influyen en ellos, hasta el origen de la diversidad fenotípica inter e intraespecífica. El objetivo de la presente tesis es indagar en el origen de la biodiversidad estudiando los patrones de diversificación de los anfibios neotropicales. El Neotrópico, la bioregión comprendida por Sudamérica, Centroamérica, el Caribe y algunas zonas del sur de Norteamérica, alberga hasta el 50% de las especies de anfibios y algunas de las familias más diversas de anuros. Su diversidad reconocida está además en continua expansión, siendo la región en la cual más especies se describen cada año, en gran parte por las especies crípticas. Más concretamente, la tesis centra su estudio en las ranas de la familia Centrolenidae y las ranas caribeñas del género Eleutherodactylus, para analizar sus patrones de diversificación haciendo uso de métodos comparados filogenéticos en combinación con datos genéticos, ecológicos, climáticos, comportamentales y bioacústicos. En el capítulo 1 se evalúa la Integrated Evolutionary Speed Hypothesis, una explicación mecanística del gradiente latitudinal de especies en la familia Centrolenidae. Usando un método comparado Bayesiano, se analiza la correlación de la tasa de evolución molecular en genes nucleares y mitocondriales con la temperatura, la altitud, la latitud, la productividad ambiental y la disponibilidad de agua, así como su relación con la tasa de diversificación, controlando los posibles efectos del tamaño corporal y la radiación UV-B. Los resultados muestran que la temperatura se encuentra asociada positivamente con la tasa de evolución molecular. Se observa además una correlación positiva entre la tasa de evolución molecular mitocondrial y la tasa de diversificación. Ambas correlaciones apoyan dos de las predicciones claves de la Integrated Evolutionary Speed Hypothesis, sin embargo, la ausencia de correlación entre la temperatura y la tasa de diversificación, así como el escaso efecto detectado sobre ella de la tasa de evolución molecular destacan el importante papel que pueden jugar otros factores (tiempo, heterogeneidad espacial o tamaños poblacionales) en el origen y mantenimiento del gradiente latitudinal de diversidad de especies. En el capítulo 2 se analiza la extraordinaria diversificación de las ranas del género Eleutherodactylus en el Caribe, con más de 160 especies ocupando muy diversos hábitats. Para ello se elabora la mayor filogenia calibrada del grupo y se reconstruye su patrón de colonización de las islas. A la luz de las relaciones filogenéticas, se analiza la morfología de más de 1700 especímenes pertenecientes a 148 especies, permitiendo evaluar si ha existido convergencia morfológica entre las especies que ocupan hábitats similares. Los resultados indican que los Eleutherodactylus caribeños se han diversificado de manera independiente en las diversas islas, convergiendo morfológicamente por adaptación a los diversos hábitats y dando lugar a distintos ecomorfos. La diversificación de Eleutherodactylus en el Caribe es por tanto fruto de radiaciones adaptativas replicadas, aparentemente resultado de la oportunidad ecológica derivada de colonizar un archipiélago sin otros competidores y de las características intrínsecas del taxón, como su desarrollo directo, lo cual facilita la dispersión por tierra y la explotación de los hábitats terrestres. En el capítulo 3 se estudia el dimorfismo sexual en tamaño en los Eleutherodactylus caribeños. Tras examinar más de 1662 individuos adultos de 139 especies, los resultados muestran un intenso dimorfismo sexual en tamaño sesgado hacia las hembras y que dicho patrón incumple la conocida como Regla de Rensch, al incrementarse la diferencia entre las hembras y los machos conforme aumenta el tamaño medio de la especie. El patrón observado parece ser fruto de la selección por fecundidad, ya que el dimorfismo se incrementa con el tamaño de las puestas debido al aumento del tamaño de las hembras. No se observa ninguna relación entre el dimorfismo sexual en tamaño y el microhábitat de las especies pero sí con el cuidado paternal. Los machos que cuidan las puestas suelen ser de mayor tamaño, reduciendo las diferencias con las hembras, que, sin embargo, continúan siendo de mayor tamaño. La existencia del dimorfismo sexual muestra la capacidad de evolución en cierta medida independiente de ambos sexos, facilitando la adaptación de machos y hembras a sus distintos óptimos selectivos. En el capítulo 4 se evalúa la existencia de especies crípticas en la especie cubana Eleutherodactylus glamyrus desde la aproximación multidisciplinar que representa la Taxonomía Integrativa. Los análisis genéticos mitocondriales y nucleares muestran el aislamiento de la población oriental, circunscrita al Pico El Gato, con respecto a las poblaciones occidentales de la Sierra Maestra. Una diferenciación genética concordante con las diferencias detectadas a nivel bioacústico (duración del canto, tiempo de ascenso, frecuencia dominante y modulación) y morfológico (en tamaño). El conjunto de resultados permite considerar a las poblaciones como linajes evolutivamente independientes y, por ello, se describe y nombra como Eleutherodactylus cattus a los especímenes de la población de Pico el Gato, poniendo de manifiesto la importancia de combinar diferentes fuentes de información para la delimitación de especies y para comprender la diversificación de linajes. Los resultados globales de la tesis revelan el origen multifactorial de la biodiversidad en anfibios. Los patrones de diversificación se ven influenciados por factores extrínsecos; como la temperatura, la biogeografía o la heterogeneidad espacial; cualidades intrínsecas de los taxones, como su capacidad de dispersión, de explotar nuevos hábitats o para evolucionar mediante la adaptación; así como el factor tiempo. Además, los resultados revelan que la diversidad puede existir oculta frente a nuestros ojos y resaltan la utilidad de la Taxonomía Integrativa para descubrirla. Seguir apostando por conocer la biodiversidad y comprender los procesos de diversificación es una tarea imprescindible y urgente en vista de la crisis ambiental que afronta nuestro planeta

A test of the Integrated Evolutionary Speed Hypothesis in a Neotropical amphibian radiation

Aim The Evolutionary Speed Hypothesis is a mechanistic explanation for the latitudinal biodiversity gradient. The recently extended Integrated Evolutionary Speed Hypothesis (IESH) proposes that temperature, water availability, population size and spatial heterogeneity influence rates of molecular evolution which, in turn, affect diversification. However, the evidence for some of the associations predicted by the IESH is not conclusive and in some cases, contradictory. Location Neotropics Methods Using a comparative Bayesian method we tested the following predictions of the IESH: the association between rate of molecular evolution and temperature (and elevation and latitude, as proxies), water availability (using precipitation and relative humidity as proxies), productivity, and rate of diversification. We also accounted for the potential confounding effects of body size and UVB radiation. We tested these predictions separately in mitochondrial and nuclear genes. Results Substitution rates of mitochondrial and nuclear genes were positively associated with temperature and negatively with elevation, while only the mitochondrial coding gene rate was associated with UVB radiation. However, when controlling for temperature, the association between substitution rate and elevation and UVB radiation disappeared, while a negative association with precipitation emerged. Moreover, diversification events were positively correlated with the rate of molecular evolution but only in mitochondrial genes. Main conclusions Our results support two key predictions of the IESH. They highlight the important association between rate of molecular evolution and temperature within a recently diverged group and also confirm the positive association between molecular evolution and diversification rate, although only in mitochondrial genes. However, the lack of association between diversification and temperature and low effect size of the relationship between substitution rates and diversification in mitochondrial genes emphasize the important role other factors, such as time, spatial heterogeneity and population size might have in the origin and maintenance of the latitudinal biodiversity gradient.Peer reviewe

Data from: Ecomorphological convergence in Eleutherodactylus frogs: a case of replicate radiations in the Caribbean

Replicate radiations, the repeated multiplication of species associated with ecological divergence, have attracted much attention and generated as much debate. Due to the few well‐studied cases, it remains unclear whether replicate radiations are an exceptional result of evolution or a relatively common example of the power of adaptation by natural selection. We examined the case of Eleutherodactylus frogs, which radiated in the Caribbean islands resulting in more than 160 species that occupy very diverse habitats. A time‐calibrated phylogeny revealed that these frogs independently diversified on all larger islands producing species that occupy a broad range of microhabitats in different islands. Using phylogenetic comparative methods, we found an association between morphological traits and particular microhabitats, and for most microhabitats detected significant morphological convergence. Our results indicate Caribbean Eleutherodactylus are a novel example of replicate radiations, and highlight the predictability of evolutionary processes, as similar ecological opportunities can lead to similar outcomes

Eleutherodactylus' morphological data

This data file includes the following species-mean values for each Eleutherodactylus species for the following traits: natural logarithm of snout-vent length (ln_SVL) and residuals of head width (res_HW), tympanum length (res_TyL), forearm length (res_FaL), hand length (res_HaL), total finger length (res_TF), total finger pad width (res_TFP), total limb length (res_TLL), total toe length (res_TT) and total toe pad width (res_TTP). Please see the article for further information

The limits to ecological limits to diversification

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification, i.e., ecological limits to diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence their diversification? In other words: are there phylogenetic limits to these ecological limits? Islands form ideal systems to answer these questions, because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, which we term clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all species regardless of their ancestry, i.e. diversity-dependence applies both to species within the same clade and between different clades. We call this island-wide (IW) diversity-dependence. Here we present a method to compute a likelihood for this model and develop a statistical procedure based on likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes which are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e. IW diversity-dependence. But it could also be suggestive of only within-clade interactions, because between-clade interactions would have blocked the same ecotype re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations, while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to ecological limits to diversification. We discuss how our new IW model advances our understanding also in other ways, ranging from identifying priority effects to modelling the spread of an epidemic in island-like systems, such as schools or hospitals

Diversification dynamics in Caribbean rain frogs ( Eleutherodactylus ) are uncoupled from the anuran community and consistent with adaptive radiation

Adaptive radiation is proposed to play a key role in generating differences in species richness among lineages and geographical regions. Due to the importance of ecological divergence in adaptive radiation, species richness is predicted to be influenced by equilibrium diversity dynamics, although the concept continues to generate much debate. An additional important question is whether radiating clades have intrinsic biological characteristics that make them particularly prone to diversify. We tackle these questions by analysing (i) the temporal patterns of diversification of Caribbean Eleutherodactylus frogs, and (ii) assembly of the complete native anuran community of the Caribbean archipelago (197 species), testing for the presence of equilibrium dynamics and whether diversification patterns of Eleutherodactylus differ from those of the rest of the Caribbean anurans. Diversification rates follow the predicted pattern of rapid diversification early in the radiation which gradually decreases towards the present. Eleutherodactylus diversification is significantly faster than that of the Caribbean anuran community, and although equilibrium dynamics influence richness of all Caribbean anurans, Eleutherodactylus shows higher carrying capacity. Our results indicate that ecological opportunity per se is not sufficient for adaptive radiation and that diverse lineages present intrinsic characteristics that enable them to make the most of available opportunity

Cryptic within cryptic: genetics, morphometrics, and bioacoustics delimitate a new species of Eleutherodactylus (Anura: Eleutherodactylidae) from Eastern Cuba

We studied the variation in genetics, bioacustics, and morphology in Eleutherodactylus glamyrus, a regionally endemic frog species restricted to high elevations in the Sierra Maestra Massif, Western Cuba that was originally described as a cryptic species hidden under the name E. auriculatus. Genetic analysis of mtDNA sequences of the 16S and cob genes identify two allopatric and strongly supported mitochondrial clades (phylogroups) which also showed no haplotype sharing in the nuclear Rag-1 gene. Bioacustic, and morphological comparisons concordantly identify these two phylogroups as independent evolutionary lineages. Therefore, we herein restrict the name Eleutherodactylus glamyrus Estrada and Hedges to populations represented in our analyses as the western phylogroup (Cordillera del Turquino to Pico La Bayamesa) and consider specimens from the eastern phylogroup (Sierra del Cobre) to represent a new species described and named as Eleutherodactylus cattus. Our results add to the growing list of Eleutherodactylus species endemic to Cuba and highlight the importance of combining different sources of evidence for obtaining robust assessments of species limits in amphibians.Fieldwork was partially funded by the Deutsche Gesellschaft für Herpetologie und Terrarienkunde (DGHT). The IdeaWild foundation provided important recording equipment. A substantial part of the work of AR was supported by a Georg Forster Fellowship from the Alexander von Humboldt Foundation. Analyses partially funded by a grant from the Spanish government, Ministerio de Economía y Competitividad, to C.V. (CGL2013-47547-P)