Using stable isotopes to determine migratory connectivity in birds: extent and limitations

La necesidad de determinar la conectividad migratoria en diversas especies de aves ha generado el surgimiento de numerosas técnicas de marcado para determinar el origen geográfico de individuos. El uso de la composición de isótopos estables en tejidos animales es una de las técnicas que más se desarrollaron en los últimos tiempos. Su uso se basa, primero, en que los valores isotópicos de diferentes elementos químicos varían espacialmente debido a procesos naturales y de origen humano. Segundo, en que un individuo, al alimentarse, asimila y eventualmente refleja en sus tejidos la composición isotópica del sitio donde se está alimentando. El tejido más utilizado en este tipo de análisis es el de las plumas remeras, ya que, al crecer, asimilan la composición isotópica del alimento, y luego permanecen metabolicamente inactivas hasta el próximo evento de muda. Aunque esta técnica ha sido exitosamente aplicada en distintas especies de aves, la variabilidad observada entre individuos limita de cierta forma su precisión. Esta variabilidad puede ser producto de diferentes procesos que afectan el cambio isotópico entre la dieta y los tejidos de la especie de interés, de desplazamientos durante el periodo de muda o de variaciones en la línea de base isotópica (cambios en los valores isotópicos de hidrógeno en las precipitaciones). Conocer y entender las fuentes de error puede ayudar a diseñar mejores estudios que minimicen la variabilidad y a desarrollar mejores modelos predictivos para determinar el origen geográfico de un individuo.The need to unravel migratory connectivity in different bird species has generated the development of several techniques to determine the geographical origin of individuals. Using the stable isotopes composition of animal tissues is one of the emerging techniques that had the greatest development. The principles of the technique are, first, that there is a geographical pattern in stable isotopes values, as a result of natural and anthropogenic processes, and, second, that stable isotopes are assimilated when an organism eats, and eventually they become fixed in animal tissues, in proportions related to the natural abundance in the environment. The most commonly used tissue is from flight feathers, since they incorporate the stable isotope composition of the food and, once moult is finished, they stay metabolically inactive until they are replaced. Although this technique has been applied with success in several species, variability found within birds from the same origin limits its potential accuracy. This variability could be the result of different processes affecting the isotopic change between food and tissues of the target species, winter movements, or baseline changes through time (temporal changes in the hydrogen isotopic values in precipitation). A better understanding of the sources of error would help to design better studies in order to minimize variability and to develop better models to determine the geographic origin of individual birds

Habitat light sets the boundaries for the rapid evolution of cichlid fish vision, while sexual selection can tune it within those limits

Cichlid fishes’ famous diversity in body coloration is accompanied by a highly diverse and complex visual system. Although cichlids possess an unusually high number of seven cone opsin genes, they express only a subset of these during their ontogeny, accounting for their astonishing interspecific variation in visual sensitivities. Much of this diversity is thought to have been shaped by natural selection as cichlids inhabit a variety of habitats with distinct light environments. Also, sexual selection might have contributed to the observed visual diversity, and sexual dimorphism in coloration potentially co‐evolved with sexual dimorphism in opsin expression. We investigated sex‐specific opsin expression of several cichlids from Africa and the Neotropics and collected and integrated datasets on sex‐specific body coloration, species‐specific visual sensitivities, lens transmission and habitat light properties for some of them. We comparatively analyzed this wide range of molecular and ecological data, illustrating how integrative approaches can address specific questions on the factors and mechanisms driving diversification, and the evolution of cichlid vision in particular. We found that both sexes expressed opsins at the same levels ‐ even in sexually dimorphic cichlid species – which argues against coevolution of sexual dichromatism and differences in sex‐specific visual sensitivity. Rather, a combination of environmental light properties and body coloration shaped the diversity in spectral sensitivities among cichlids. We conclude that although cichlids are particularly colorful and diverse and often sexually dimorphic, it would appear that natural rather than sexual selection is a more powerful force driving visual diversity in this hyper‐diverse lineage

Asymmetry in genitalia is in sync with lateralized mating behavior but not with the lateralization of other behaviors

Asymmetries in bilateral organisms attract a lot of curiosity given that they are conspicuous departures from the norm. They allow the investigation of the integration at different levels of biological organization. Here we study whether and how behavioral and asymmetrical anatomical traits co-evolved and work together. We ask if asymmetry is determined locally for each trait or at a whole individual level in a species bearing conspicuous asymmetrical genitalia. Asymmetric genitalia evolved in many species; however, in most cases the direction of asymmetry is fixed. Therefore, it has been rarely determined if there is an association between the direction of asymmetry in genitalia and other traits. In onesided livebearer fish of the genus Jenynsia (Cyprinodontiformes, Anablepidae), the anal fin of males is modified into a gonopodium, an intromittent organ that serves to inseminate females. The gonopodium shows a conspicuous asymmetry, with its tip bending either to the left or the right. By surveying 13 natural populations of Jenynsia lineata, we found that both genital morphs are equally common in wild populations. In a series of experiments in a laboratory population, we discovered asymmetry and lateralization for multiple other traits; yet, the degree of integration varied highly among them. Lateralization in exploratory behavior in response to different stimuli was not associated with genital morphology. Interestingly, the direction of genital asymmetry was positively correlated with sidedness of mating preference and the number of neuromasts in the lateral line. This suggests integration of functionally linked asymmetric traits; however, there is no evidence that asymmetry is determined at the whole individual level in our study species.Fil: Torres Dowdall, Julián Roberto. Universität Konstanz; AlemaniaFil: Rometsch, Sina J.. Universität Konstanz; AlemaniaFil: Aguilera, Gaston. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; Argentina. Fundación Miguel Lillo. Dirección de Zoología. Instituto de Vertebrados. Sección Ictiología; ArgentinaFil: Goyenola, Guillermo. Universidad de la Republica. Centro Universitario Regional del Este.; UruguayFil: Meyer, Axel. Universität Konstanz; Alemani

Molecular and morphological convergence to sulfide-tolerant fishes in a new species of Jenynsia (Cyprinodontiformes: Anablepidae), the first extremophile member of the family

Freshwater sulfide springs have extreme environmental conditions that only few vertebrate species can tolerate. These species often develop a series of morphological and molecular adaptations to cope with the challenges of life under the toxic and hypoxic conditions of sulfide springs. In this paper, we described a new fish species of the genus Jenynsia, Anablepidae, from a sulfide spring in Northwestern Argentina, the first in the family known from such extreme environment. Jenynsia sulfurica n. sp. is diagnosable by the lack of scales on the pre-pelvic area or the presence of a single row of scales, continuous or not, from the isthmus to the bases of the pelvic fins. Additionally, it presents a series of morphological and molecular characteristics that appear convergent with those seen in other fish species (e.g., Poeciliids) inhabiting sulfide springs. Most notably, J. sulfurica has an enlarged head and postorbital area compared to other fish of the genus and a prognathous lower jaw with a hypertrophied lip, thought to facilitate respiration at the air-water interface. Analyses of cox1 sequence showed that J. sulfurica has two unique mutations resulting in amino acid substitutions convergent to those seen in Poeciliids from sulfide springs and known to provide a physiological mechanism related to living in sulfide environments. A phylogenetic analysis, including molecular and morphological characters, placed J. sulfurica as sister taxa to J. alternimaculata, a species found in nearby, non-sulfide habitats directly connected to the sulfide springs. Thus, it can be inferred that the selection imposed by the presence of H2S has resulted in the divergence between these two species and has potentially served as a barrier to gene flow.Fil: Aguilera, Gastón. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Teran, Guillermo Enrique. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Mirande, Juan Marcos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Alonso, Felipe. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Salta. Instituto de Bio y Geociencias del NOA. Universidad Nacional de Salta. Facultad de Ciencias Naturales. Museo de Ciencias Naturales. Instituto de Bio y Geociencias del NOA; ArgentinaFil: Rometsch, Sina. University Of Konstanz, Germany; AlemaniaFil: Meyer, Axel. University Of Konstanz, Germany; AlemaniaFil: Torres Dowdall, Julián Roberto. University Of Konstanz, Germany; Alemania. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas, Físicas y Naturales. Centro de Zoología Aplicada; Argentin

Molecular and morphological convergence to sulfide-tolerant fishes in a new species of Jenynsia (Cyprinodontiformes: Anablepidae), the first extremophile member of the family

Freshwater sulfide springs have extreme environmental conditions that only few vertebrate species can tolerate. These species often develop a series of morphological and molecular adaptations to cope with the challenges of life under the toxic and hypoxic conditions of sulfide springs. In this paper, we described a new fish species of the genus Jenynsia, Anablepidae, from a sulfide spring in Northwestern Argentina, the first in the family known from such extreme environment. Jenynsia sulfurica n. sp. is diagnosable by the lack of scales on the pre-pelvic area or the presence of a single row of scales, continuous or not, from the isthmus to the bases of the pelvic fins. Additionally, it presents a series of morphological and molecular characteristics that appear convergent with those seen in other fish species (e.g., Poeciliids) inhabiting sulfide springs. Most notably, J. sulfurica has an enlarged head and postorbital area compared to other fish of the genus and a prognathous lower jaw with a hypertrophied lip, thought to facilitate respiration at the air-water interface. Analyses of cox1 sequence showed that J. sulfurica has two unique mutations resulting in amino acid substitutions convergent to those seen in Poeciliids from sulfide springs and known to provide a physiological mechanism related to living in sulfide environments. A phylogenetic analysis, including molecular and morphological characters, placed J. sulfurica as sister taxa to J. alternimaculata, a species found in nearby, non-sulfide habitats directly connected to the sulfide springs. Thus, it can be inferred that the selection imposed by the presence of H2S has resulted in the divergence between these two species and has potentially served as a barrier to gene flow.Fil: Aguilera, Gastón. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Teran, Guillermo Enrique. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Mirande, Juan Marcos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Alonso, Felipe. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Salta. Instituto de Bio y Geociencias del NOA. Universidad Nacional de Salta. Facultad de Ciencias Naturales. Museo de Ciencias Naturales. Instituto de Bio y Geociencias del NOA; ArgentinaFil: Rometsch, Sina. University Of Konstanz, Germany; AlemaniaFil: Meyer, Axel. University Of Konstanz, Germany; AlemaniaFil: Torres Dowdall, Julián Roberto. University Of Konstanz, Germany; Alemania. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas, Físicas y Naturales. Centro de Zoología Aplicada; Argentin

Intra- and interspecific variation along environmental gradients: adaptation, plasticity, and range limits

2012 Spring.Includes bibliographical references.Understanding the processes underlying patterns of intraspecific variation, and how these processes in turn shape the distributional limits of species is a fundamental goal of evolutionary ecology. The study of species distributed along environmental gradients provides a framework for testing how changing conditions lead to local adaptation, phenotypic plasticity, and ultimately shape distributional limits. Yet, environmental gradients are complex, being composed of a diversity of abiotic and biotic factors that act on individual species and shape the interactions between them. Thus, empirical studies aimed to understand patterns of intraspecific divergence and interspecific diversity need to evaluate the effects of both abiotic and biotic factors varying along gradients. Evolutionary ecologists have become increasingly interested in trying to understand the costs and limits to trait variation along environmental gradients and what factors prevent species from evolving larger geographic ranges. Theory predicts that species distributed along environmental gradients should track conditions through local adaptation or adaptive phenotypic plasticity, and that a disruptive factor along the gradient (e.g. increase in the steepness of the gradient, the presence of a competitor, etc.) could result in the formation of distribution limits as conditions become unsuitable for populations persistence. Empirical studies analyzing large-scale patterns of phenotypic variation have provided support for the formation of clines in response to environmental gradients. However, less evidence has accumulated for the formation of such patterns at local scales and clear disruptive factors leading to distributional limits remain elusive. My dissertation takes an evolutionary ecological perspective to understand how environmental gradients shape patterns of variation within and between species. Here, I attempt to understand how abiotic and biotic factors interact to drive patterns of phenotypic variation. To approach this question, I used as a study system two closely related, ecologically similar, and parapatric species of poeciliids distributed along rivers on the island of Trinidad, West Indies. In the first part of this dissertation, I focus on the patterns of intraspecific variation in the Trinidadian guppy (Poecilia reticulata) along a predation risk gradient. I used this species to explore the spatial scale at which local adaptation occurs (Chapter 1), and to investigate the role of adaptive phenotypic plasticity in allowing species to track local optima (Chapter 2). I found that local adaptation in Trinidadian guppies occurs at a smaller spatial scale than previously shown. My results also suggest that adaptive plasticity plays an important role in allowing Trinidadian guppies to track local optima along a gradient of predation risk. Furthermore, I found divergence in patterns of plasticity between Trinidadian guppy populations adapted to low- or to high-levels of predation pressure. My results suggest that this difference in adaptive phenotypic plasticity evolved as a by-product of adaptation to local environmental conditions. In the second part of my dissertation I change my focus from patterns of intraspecific variation to patterns of interspecific variation along environmental gradients. I examine how the Trinidadian guppy and its sister species, the swamp guppy (P. picta), are distributed along a complex environmental gradient in lowland rivers of Trinidad (Chapter 3), and performed a series of experiments aimed to determine what factors drive their distributions (Chapter 4). As Trinidadian rivers approach the ocean, several factors change in comparison to upstream localities, including changes in productivity, physicochemical conditions, and community composition. I found that the Trinidadian guppy and the swamp guppy show an overlapping parapatric distribution along the interface between brackish-freshwater in the lowland rivers of Trinidad. The swamp guppy is usually found in downstream sections of the rivers, both in fresh- and brackish water. On the other hand, the Trinidadian guppy is only found in freshwater, dropping off abruptly at the brackish-freshwater interface. Field and laboratory experiments suggest that brackish water environments are physiologically stressful for the two study species, as survival and growth rate in this environment were lower compared to that observed in freshwater. Also, these experiments indicate that the Trinidadian guppy is competitively dominant over the swamp guppy across all salinity conditions. Thus, I showed that asymmetric competition limits the competitively subordinate swamp guppy to the harshest end of the salinity gradient, and that stressful salinity conditions limits the dominant Trinidadian guppy to the less stressful freshwater end of the gradient

Convergent phenotypic evolution of the visual system via different molecular routes : how Neotropical cichlid fishes adapt to novel light environments

How predictable is evolution? This remains a fundamental but contested issue in evolutionary biology. When independent lineages colonize the same environment, we are presented with a natural experiment that allows us to ask if genetic and ecological differences promote species‐specific evolutionary outcomes or whether species phenotypically evolve in a convergent manner in response to shared selection pressures. If so, are the molecular mechanisms underlying phenotypic convergence the same? In Nicaragua, seven species of cichlid fishes concurrently colonized two novel photic environments. Hence, their visual system represents a compelling model to address these questions, particularly since the adaptive value of phenotypic changes is well‐understood. By analyzing retinal transcriptomes, we found that differential expression of genes responsible for color vision (cone opsins and cyp27c1) produced rapid and mostly convergent changes of predicted visual sensitivities. Notably, these changes occurred in the same direction in all species although there were differences in underlying gene expression patterns illustrating nonconvergence at the molecular level. Adaptive phenotypes evolved deterministically, even when species differ substantially in ecology and genetic variation. This provides strong evidence that phenotypic evolution of the visual system occurred in response to similar selective forces of the photic environment.publishe

Evolutionary dynamics of pre- and postzygotic reproductive isolation in cichlid fishes

Cichlid fishes are exceptionally species-rich, speciated at explosive rates and, hence, are a model system in speciation research. Yet, their reproductive isolating barriers have, so far, not been comprehensively studied. Here, we review current knowledge on pre- and postzygotic mechanisms in cichlids. While premating isolation is the norm in cichlids, its strength varies across lineages and with the geographical setting. Moreover, manipulations of ambient conditions tended to reduce assortative mating among closely related species, suggesting that premating isolation in cichlids is often fragile and context dependent. The observed lack of complete reproductive isolation is supported by past and present hybridization events that have contributed to diversity by creating novel allelic combinations. On the other hand, our meta-analysis highlights that intrinsic postzygotic isolation might accumulate faster than assumed. Mild forms of genetic incompatibilities, such as sex ratio distortion, can already be observed among closely related species. Therefore, cessation of gene flow by strong reproductive isolation in cichlids requires a combination of premating prezygotic isolation supplemented with intrinsic and extrinsic postzygotic barriers. Further, we suggest crucial next steps to improve our knowledge about reproductive barriers in cichlids to understand the evolutionary dynamics of pre- and postzygotic isolation mechanisms during adaptive radiations. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.publishe

Rapid and parallel adaptive evolution of the visual system of Neotropical Midas cichlid fishes

Midas cichlid fish are a Central American species flock containing 13 described species that has been dated to only few thousand years old, a historical timescale infrequently associated with speciation. Their radiation involved the colonization of several clear water crater lakes from two turbid great lakes. Therefore, Midas cichlids have been subjected to widely varying photic conditions during their radiation. Being a primary signal relay for information from the environment to the organism, the visual system is under continuing selective pressure and a prime organ system for accumulating adaptive changes during speciation, particularly in the case of dramatic shifts in photic conditions. Here, we characterize the full visual system of Midas cichlids at organismal and genetic levels, to determine what types of adaptive changes evolved within the short time span of their radiation. We show that Midas cichlids have a diverse visual system with unexpectedly high intra- and interspecific variation in color vision sensitivity and lens transmittance. Midas cichlid populations in the clear crater lakes have convergently evolved visual sensitivities shifted towards shorter wavelengths compared to the ancestral populations from the turbid great lakes. This divergence in sensitivity is driven by changes in chromophore usage, differential opsin expression, opsin coexpression, and to a lesser degree by opsin coding sequence variation. The visual system of Midas cichlids has the evolutionary capacity to rapidly integrate multiple adaptations to changing light environments. Our data may indicate that, in early stages of divergence, changes in opsin regulation could precede changes in opsin coding sequence evolution