Mechanisms of adaptation to a changing world

Programa de Doctorado en Medio Ambiente y SociedadLínea de Investigación: Biodiversidad y Biología de la ConservaciónClave Programa: DAMCódigo Línea: 83The current extinction rate of species on Earth is greater than any of the mass extinctions registered in the fossil record in its entire history. This increased biodiversity loss is caused one way or the other by the human species. Changes in land use, climate or biological invasions are acting worldwide. In this context, understanding the mechanisms by which organisms adapt to the environment and the ecological and evolutionary consequences that these entail is a key factor. In this thesis, this question is approached from two different perspectives. The first one (Section 1) assesses how populations of invasive species adapt to a new environment. Before a population becomes invasive in a non-native area, it must first have passed through the earlier stages of invasion (capture, transport and introduction) before their establishment in this area. These stages could be acting as selective filters of individual variation. In this way, the introduced individuals would not be a random sub-sample of the native population of origin. This could have a great impact on their invasive potential. However, what happens in these earliest invasion stages has hardly ever been studied. To test the hypothesis that selection acts already early during a biological invasion, we followed the individuals of two invasive bird species from their native habitat in Senegal and during these early stages of a potential invasion. We indeed found that selection acts on variation in a gene related to behaviour (Chapter I). In addition, we found that selection also acts on many other phenotypic characteristics that could have a great importance for invasive potential, such as sex, age, body size, brain size, beak size and shape, body condition, stress hormone levels and behaviour (Chapter II). The second perspective (Section 2) assesses how native populations adapt to environmental changes. For this we studied all the possible mechanisms of adaptation (natural selection, phenotypic plasticity, habitat choice and environment adjustment), but especially focusing on matching habitat choice. This mechanism is based on the non-random dispersal of individuals due to an assessment of variation in their local performance, such that individuals settle down in those habitats that best match their phenotypes. Despite its eco-evolutionary importance, this mechanism has received almost no research attention. In this thesis, we study how a native population of grasshoppers has adapted in camouflage (a classic form of adaptation to the environment) in the colonization of a new urban environment (one of the most drastic changes in the habitat). We found a population divergence on a micro-geographic scale (differently coloured grasshoppers on distinctly coloured urban substrates) despite the existence of a lot of (presumably homogenising) movement by individuals. In Chapter III, we demonstrate that habitat choice, and not other mechanisms such as natural selection or phenotypic plasticity, is the main mechanism that has caused the recent local evolution of camouflage and the micro-geographic population divergence. In addition, we find that habitat choice acts also at a much finer scale, in which individuals improve their camouflage by aligning with certain substrate patterns depending on their degree of colour matching with the substrate, making it a flexible way to increase performance on different spatial scales (Chapter IV). However, this matching between phenotype and environment can also be achieved through phenotypic plasticity. In Chapter V we show that grasshoppers are able to change their body coloration through successive moults to resemble the substrate on which they live. The degree to which they do so is affected by the risk of predation they are exposed to: experimental increase of risk resulted in an increased phenotypic adjustment. Taken together, this thesis demonstrates in a convincing and quantitative manner the existence and importance of two neglected mechanisms of adaptation of populations to environmental changes, thereby increasing our understanding of how invasive and native populations adapt to change and ecological opportunities in an increasingly changing world.La tasa de extinción actual de las especies en la Tierra es mayor que cualquiera de las extinciones masivas registradas en el registro fósil en toda su historia. Esta mayor pérdida de biodiversidad es causada de una manera u otra forma por la especie humana. Los cambios en el uso de la tierra, el clima o las invasiones biológicas actúan de forma global. En este contexto, entender los mecanismos por los cuales los organismos se adaptan al medio ambiente y las consecuencias ecológicas y evolutivas que implican es un factor clave. En esta tesis, esta cuestión se aborda desde dos perspectivas diferentes. La primera (Sección 1) evalúa cómo las poblaciones de especies invasoras se adaptan a un nuevo entorno. Antes de que una población sea invasora en un área no nativa, primero debe haber pasado por las etapas más tempranas de la invasión (captura, transporte e introducción) antes de su establecimiento en dicha área. Estas etapas podrían actuar como filtros selectivos de variación individual. De esta forma, los individuos introducidos no serían una sub-muestra aleatoria de la población nativa de origen. Esto podría tener un gran impacto en su potencial invasivo. Sin embargo, lo que sucede en estas primeras etapas de invasión casi nunca se ha estudiado. Para testar la hipótesis de que la selección ya actúa en las fases más tempranas durante una invasión biológica, seguimos a los individuos de dos especies de aves invasoras desde su hábitat natural en Senegal y durante estas primeras etapas de una posible invasión. De hecho, encontramos que la selección actúa sobre la variación en un gen relacionado con el comportamiento (Capítulo I). Además, encontramos que la selección también actúa sobre muchas otras características fenotípicas que podrían tener una gran importancia para el potencial invasivo, como sexo, edad, tamaño corporal, tamaño del cerebro, tamaño y forma del pico, condición corporal, niveles hormonales de estrés y comportamiento (Capitulo II). La segunda perspectiva (Sección 2) evalúa cómo las poblaciones nativas se adaptan a los cambios ambientales. Para esto estudiamos todos los posibles mecanismos de adaptación (selección natural, plasticidad fenotípica, elección del hábitat y ajuste del ambiente), pero especialmente centrándonos en la elección del hábitat correspondiente. Este mecanismo se basa en la dispersión no aleatoria de individuos debido a una evaluación de la variación en su desempeño local, de modo que los individuos se establecen en los hábitats que mejor se adaptan a sus fenotipos. A pesar de su importancia eco-evolutiva, este mecanismo casi no ha recibido atención de investigación. En esta tesis, estudiamos cómo una población nativa de saltamontes se ha adaptado en camuflaje (una forma clásica de adaptación al ambiente) en la colonización de un nuevo entorno urbano (uno de los cambios más drásticos en el hábitat). Encontramos una divergencia poblacional a escala micro-geográfica (saltamontes de diferentes colores sobre sustratos urbanos de distintos colores) a pesar de la existencia de un gran movimiento (presumiblemente homogeneizador) por parte de los individuos. En el Capítulo III, demostramos que la elección del hábitat, y no otros mecanismos como la selección natural o la plasticidad fenotípica, es el principal mecanismo que ha causado la reciente evolución local del camuflaje y la divergencia de la población a escala micro-geográfica. Además, encontramos que la elección del hábitat también actúa a una escala mucho más fina, en la que los individuos mejoran su camuflaje al alinearse con ciertos patrones de sustrato dependiendo de su grado de coincidencia de color con el sustrato, convirtiéndolo en una forma flexible de aumentar el rendimiento en diferentes escalas espaciales (Capítulo IV). Sin embargo, esta coincidencia entre el fenotipo y el medio ambiente también se puede lograr a través de la plasticidad fenotípica. En el Capítulo V mostramos que los saltamontes son capaces de cambiar la coloración de su cuerpo a través de mudas sucesivas para parecerse al sustrato en el que viven. El grado en que lo hacen se ve afectado por el riesgo de depredación a la que están expuestos: el aumento experimental del riesgo resultó en un aumento del ajuste fenotípico. En conjunto, esta tesis demuestra de manera convincente y cuantitativa la existencia e importancia de dos mecanismos poco estudiados de adaptación de las poblaciones a los cambios ambientales, aumentando nuestra comprensión de cómo las poblaciones nativas e invasoras se adaptan al cambio y las oportunidades ecológicas en un mundo cada vez más cambiante.Universidad Pablo de Olavide de Sevilla. Departamento de Biología Molecular e Ingeniería BioquímicaPostprin

Seed dispersal by macaws shapes the landscape of an Amazonian ecosystem

Seed dispersal is one of the most studied plant–animal mutualisms. It has been proposed that the dispersal of many large-seeded plants from Neotropical forests was primarily conducted by extinct megafauna, and currently by livestock. Parrots can transport large fruits using their beaks, but have been overlooked as seed dispersers. We demonstrate that three macaws (Ara ararauna, A. glaucogularis and A. severus) are the main dispersers of the large-seeded motacú palm Attalea princeps, which is the biomass-dominant tree in the Bolivian Amazonian savannas. Macaws dispersed fruits at high rates (75– 100% of fruits) to distant (up to 1200 m) perching trees, where they consumed the pulp and discarded entire seeds, contributing to forest regeneration and connectivity between distant forests islands. The spatial distribution of immature palms was positively associated to the proximity to macaws’ perching trees and negatively to the proximity to cattle paths. The disperser role of livestock, presumably a substitute for extinct megafauna, had little effect due to soil compaction, trampling and herbivory. Our results underscore the importance of macaws as legitimate, primary dispersers of large-seeded plants at long distances and, specifically, their key role in shaping the landscape structure and functioning of this Amazonian biomePeer reviewe

Field data

Field data. Grasshoppers using different strategies to improve camouflage: positioning behavior and background matching in a novel urban habita

Data from: Positioning behavior according to individual color variation improves camouflage in novel habitats

Behavior can play a key role in adaptation, especially in novel environments. Here we study how ground-perching grasshoppers that colonized street pavements as novel habitats behaviorally manage their detection rates by predators. We found that grasshoppers positioned themselves aligned with the spaces between adjacent bricks more than expected by chance. By performing a virtual predation experiment, we confirmed that this positioning behavior decreases predation rate. Surprisingly, individuals with a poorer cryptic coloration made greater use of this positioning behavior, while individuals with a better cryptic coloration relied more on background color matching. Additionally, positioning behavior interacted with other anti-predation behaviors: individuals who were positioned on the space between bricks allowed potential predators to get closer before fleeing. These results indicate that these grasshoppers showed adaptive flexibility in camouflage and escape behaviors as a function of both individual and environmental variation. Such behavioral flexibility should allow organisms to cope better with novel environments, which deserves more study especially in the current context of global change

Data from: Background colour matching increases with risk of predation in a colour-changing grasshopper

Cryptic colouration can be adjusted to the local environment by physiological (rapid) change, and/or by morphological (slow) change. The threat-sensitivity hypothesis predicts that the degree of crypsis should respond to the risk of predation (assuming some cost to crypsis). This has not been studied for morphological colour changers, so we manipulated the colour of the rearing substrate (black versus white) and the perceived risk of predation (higher versus lower) for the grasshopper Sphingonotus azurescens. Over a period of several weeks, both nymphs and adults greatly adjusted the brightness of their body towards that of the substrate. Moreover, when individuals were exposed to a greater simulated predation risk (disturbance by hand), they became even more similar in brightness to their substrates, apparently augmenting their degree of crypsis. This study on a morphological colour changer shows that the degree of cryptic colouration (body brightness) is under individual control and appears to change adaptively in response to increased predation risk. In addition, based on analyses of systematic differences in colour in lab-reared offspring, we found indications that even in colour changers there is genetic variation in colouration among individuals, and that populations have diverged adaptively. Such integration of factors determining the cryptic phenotype improves our understanding of the natural selection and constraints imposed on crypsis, which influence both its optimization and evolution

Escape-strategy data

Escape behavior data ( FID and flight distance) of grasshoppers in a urban habita

R code

R code used for statistical analyze

Virtual predation data

Data from a virtual predation experiment (in a touch screen) of grasshoppers using different strategies of camouflage and humans as predators

Seed dispersal by macaws shapes the landscape of an Amazonian ecosystem

Seed dispersal is one of the most studied plant–animal mutualisms. It has been proposed that the dispersal of many large-seeded plants from Neotropical forests was primarily conducted by extinct megafauna, and currently by livestock. Parrots can transport large fruits using their beaks, but have been overlooked as seed dispersers. We demonstrate that three macaws (Ara ararauna, A. glaucogularis and A. severus) are the main dispersers of the large-seeded motacú palm Attalea princeps, which is the biomass-dominant tree in the Bolivian Amazonian savannas. Macaws dispersed fruits at high rates (75– 100% of fruits) to distant (up to 1200 m) perching trees, where they consumed the pulp and discarded entire seeds, contributing to forest regeneration and connectivity between distant forests islands. The spatial distribution of immature palms was positively associated to the proximity to macaws’ perching trees and negatively to the proximity to cattle paths. The disperser role of livestock, presumably a substitute for extinct megafauna, had little effect due to soil compaction, trampling and herbivory. Our results underscore the importance of macaws as legitimate, primary dispersers of large-seeded plants at long distances and, specifically, their key role in shaping the landscape structure and functioning of this Amazonian biomePeer reviewe

data adults grasshoppers

data adults grasshopper