Variabilidad demográfica y de historia vital en una planta de amplia distribución: el papel de los factores medioambientales, geográficos y genéticos

Esta tesis ha sido realizada en el Instituto Pirenaico de Ecología (IPE-CSIC), con la financiación de una beca FPU del Ministerio de Educación y Ciencia a J. Villellas, la concesión de los proyectos nacionales CGL2006-08507/BOS, 018/2008 y CGL2010-21642 a M.B. García, y la colaboración de J. Ehrén, J.M. Olesen, R. Braza, W.F. Morris, R. Berjano, A. Terrab, y diversos ayudantes de campo y laboratorio.Peer reviewe

Weak relationship between neutral genetic diversity and demography in a plant at continental scale

El comportamiento demográfico de las poblaciones resulta determinante para la abundancia y distribución de las especies, por lo que identificar las causas de su variación permite una mejor gestión de la biodiversidad. Además del efecto de las condiciones ambientales, la diversidad genética puede tener consecuencias demográficas importantes, pero existe un mayor conocimiento de tales efectos en especies amenazadas que en organismos comunes. En el presente estudio se analizaron los efectos de las condiciones ambientales en la demografía de una planta de amplia distribución, Plantago coronopus, a lo largo de su rango latitudinal europeo, considerando las diferencias en diversidad genética neutral. La diversidad genética sólo mostró relación con uno de los parámetros demográficos analizados, el crecimiento individual, y no mostró ninguna influencia sobre la tasa de crecimiento poblacional. En cambio, diversos factores ambientales abióticos (clima, suelo) y bióticos (densidad poblacional) tuvieron una mayor influencia en los componentes del ciclo vital (supervivencia, crecimiento, reproducción). Estas tasas individuales presentaron respuestas opuestas entre ellas a los factores ambientales, fenómeno conocido como compensación demográfica, lo que resultó en una ausencia de patrón en la tasa de crecimiento poblacional a lo largo del gradiente ambiental. Estos resultados destacan la importancia de considerar múltiples parámetros demográficos individuales y poblacionales para evaluar de manera consistente la relación entre genética, condiciones ambientales y demografía en una especie. Nuestro estudio también sugiere que, en especies de distribución amplia, los factores genéticos pueden resultar menos útiles que las variables ambientales para predecir su comportamiento y futura distribución ante nuevos escenarios ecológicos.Population performance is determinant for the abundance and distribution of species and identifying the causes of its variation allows a better management of biodiversity. Besides the effect of environmental conditions, genetic diversity may also have significant demographic consequences, but there is greater knowledge of such effects in threatened species than in common organisms. In the present study, the influence of environmental conditions on the demography of a widespread herbaceous plant, Plantago coronopus, was analyzed throughout its European latitudinal range, considering also differences in neutral genetic diversity. Genetic diversity was only related to one of the demographic parameters analyzed, individual growth, and showed no influence on the population growth rate. In contrast, several abiotic (climate, soil) and biotic (population density) environmental factors had a greater influence on the life cycle components (survival, growth, reproduction). These individual rates showed opposite responses to environmental factors, a phenomenon known as demographic compensation, which resulted in an absence of pattern in the population growth rate along the environmental gradient. Our results highlight the importance of considering multiple individual and population demographic parameters to evaluate the relationship between a species genetics, environmental conditions, and demography. This study also suggests that, in organisms with wider distribution ranges, genetic factors may be less useful than environmental variables to predict population trends and future distribution in new ecological scenarios.Ministerio de Ciencia e Innovación de España CGL2006-08507 y CGL2010-2164

Divergence between phenotypic and genetic variation within populations of a common herb across Europe

Analyzing the pattern and causes of phenotypic and genetic variation within and among populations might help to understand life history variability in plants, and to predict their responses to changing environmental conditions. Here we compare phenotypic variation and genetic diversity of the widespread herb Plantago coronopus across Europe, and evaluate their relationship with environmental and geographical factors. Genetic diversity was estimated in 18 populations from molecular markers with AFLP. Phenotypic variation was measured in a subset of 11 populations on six life history traits (plant size, plant growth, fecundity, seed mass, mucilage production and ratio between two functionally different seed morphs). To account for ecological and geographical correlates, we estimated variability in local temperature, precipitation and intraspecific competition, and accounted for the central vs. peripheral position of populations. Phenotypic variation and genetic diversity were not significantly correlated within populations throughout the species' range. Phenotypic variation was positively linked to precipitation variability, whereas genetic diversity was correlated with the position of populations, suggesting that both types of variation are shaped by different processes. Precipitation seems to have acted as a selective agent for variation within populations in most life history traits, whereas the species' post-glacial demographic history has likely reduced genetic diversity in northern peripheral populations with respect to central ones. The positive association between precipitation variability and phenotypic variation also suggests that plant populations may have higher adaptive potential in ecologically variable rather than stable environments. Our study offers an additional criterion when predicting the future performance of species under environmental changes.Minsterio de Ciencia e Innovación (España) CGL2006-08507 CGL2010-21642 CGL2009-0871

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Demographic and life-history variability across the range of a widespread herb: the role of environmental, geographical and genetic factors / Variabilidad demográfica y de historia vital en una planta de amplia distribución: el papel de los factores medioambientales, geográficos y genéticos

[spa] Las especies de amplia distribución han recibido tradicionalmente poca atención, a pesar de su importancia para la estructura y el funcionamiento de los ecosistemas. En esta tesis, se analiza la variabilidad demográfica, de historia vital y genética en una planta de amplia distribución en Europa y el norte de África (Plantago coronopus), en un total de 22 poblaciones a lo largo de gran parte del rango latitudinal de la especie (centro y periferia norte). Se pretende analizar la magnitud y las causas de esta variabilidad intraespecífica en relación con la posición de las poblaciones dentro del rango y con los principales factores medioambientales. Las poblaciones periféricas mostraron una menor diversidad genética, pero no mostraron en general un peor o más variable comportamiento demográfico en cuanto a densidad o tasa de crecimiento poblacional, contradiciendo así las hipótesis clásicas centro-periferia. Se encontró un mismo patrón de diferenciación demográfica dentro de las regiones tanto central como periférica, en relación con la variación en el régimen de precipitaciones. La tasa de reclutamiento de nuevos individuos fue el proceso del ciclo vital con mayor importancia para el funcionamiento de las poblaciones. Se encontró también una gran variación entre poblaciones en las características de las semillas (número, tamaño, mucílago y proporción de dos tipos de semilla dimórficos) en relación con el gradiente de estrés ambiental. Finalmente, la variación fenotípica dentro de las poblaciones se relacionó con la variabilidad ambiental, mientras que la diversidad genética se correlacionó con la posición central vs. periférica de las poblaciones y posiblemente con la historia demográfica de la especie. Globalmente, este estudio muestra la importancia de distinguir entre periferia geográfica y marginalidad ecológica, y sugiere que el éxito de las plantas de amplia distribución reside en una gran variabilidad demográfica y de historia vital a diferentes escalas espaciales.[eng] Widespread species have traditionally received much less attention than rare and endemic ones. However, they are crucial in macroecological patterns and in ecosystem structure and functioning. Thus, understanding the characteristics that allow widespread organisms to extend over large areas has a high interest from both theoretical and applied perspectives. One of the most frequent hypotheses to explain the success of widespread plants is that they show much wider ecological niches, and thus a high life-history and demographic variability. However, studies are often very specific and carried out over small spatio-temporal scales, which hinders a general understanding of intraspecific variation in widespread taxa. In this thesis, we span a large spatio-temporal scale and a large environmental gradient to analyze the magnitude and the possible causes of natural variation in the in the range centre and the northern periphery of the widespread herb Plantago coronopus. More precisely, we analyze variability in population dynamics, life-history traits, and genetic diversity in up to 22 populations in Europe and North Africa. We aim to explore the relation of such variability with the position of populations within the species’ range, since peripheral populations are traditionally expected to show a lower and more variable performance with respect to central populations. Additionally, we aim to analyze the effects of the most relevant environmental factors in population and individual performance at different spatial scales. In the first chapter, we found higher values in central populations in some vital rates, such as fecundity and growth, but recruitment and density were higher in northern peripheral populations, and there were no clear differences between regions in temporal variability of vital rates. Differences in population performance across the species’ range seemed to be correlated with local precipitation and intraspecific competition. In the second chapter, differences in mean values and variability of vital rates between central and peripheral areas led to no differences in stochastic population growth rates. In addition, recruitment was the most influential vital rate for population growth rates at different spatial scales, and we found the same pattern of differentiation in population dynamics in response to environmental conditions within central and peripheral regions. In the third chapter, we reported high variation among populations in seed traits along a steep environmental stress gradient. Moreover, patterns in seed production were opposite at the fruit and the individual scale, as a strategy of populations to maximize fitness in each set of local conditions. Finally, in the fourth chapter, we found no relationship within populations between phenotypic variability and genetic diversity. Phenotypic variation was mainly shaped by precipitation variability, suggesting adaptive variation, whereas genetic diversity was correlated with the central vs. peripheral position, probably in close relation with some random demographic processes experienced by populations in the past. Despite genetic diversity was higher in central populations, our results contradicted classical hypotheses predicting a lower demographic performance towards species’ range edges. In fact, environmental conditions seemed to have a higher influence on plant performance than the position of populations within the species’ range, which calls for the necessity of distinguishing between geographical periphery and ecological marginality in demographic studies. Overall, our study highlights the versatility of P. coronopus at different spatial scales in response to varying environmental conditions, complementing similar findings of previous research on the same taxon at smaller spatial scales. Such life-history variability seems to be a key factor for widespread plants to extend over large and heterogeneous ranges

Geographic location, local environment, and individual size mediate the effects of climate warming and neighbors on a benefactor plant

Predictions of plant responses to global warming frequently ignore biotic interactions and intraspecific variation across geographical ranges. Benefactor species play an important role in plant communities by protecting other taxa from harsh environments, but the combined effects of warming and beneficiary species on their performance have been largely unexamined. We analyzed the joint effects of elevated temperature and neighbor removal on the benefactor plant Silene acaulis, in factorial experiments near its low- and high-latitude range limits in Europe. We recorded growth, probability of reproduction and fruit set during 3 years. The effects of enhanced temperature were positive near the northern limit and negative in the south for some performance measures. This pattern was stronger in the presence of neighbors, possibly due to differential thermal tolerances between S. acaulis and beneficiary species in each location. Neighbors generally had a negative or null impact on S. acaulis, in agreement with previous reviews of overall effects of plant–plant interactions on benefactors. However, small S. acaulis individuals in the north showed higher growth when surrounded by neighbors. Finally, the local habitat within each location influenced some effects of experimental treatments. Overall, we show that plant responses to rising temperatures may strongly depend on their position within the geographic range, and on species interactions. Our results also highlight the need to consider features of the interacting taxa, such as whether they are benefactor species, as well as local-scale environmental variation, to predict the joint effects of global warming and biotic interactions on species and communities.This project was funded by the Swedish Research Council to W. F. Morris (Ref: 2012-42619-94710-26) and by the Spanish Ministry of Economy, Industry and Competitiveness to M. B. García (CGL2017-90040-R)

Variation in stochastic demography between and within central and peripheral regions in a widespread short-lived herb

36 páginas, 4 figuras.[EN] Analyzing intraspecific variation in population dynamics in relation to environmental factors is crucial to understand the current and future distributions of plant species. Across ranges, peripheral populations are often expected to show lower and more temporally variable vital rates than central populations, although it remains unclear how much any differences in vital rates actually contribute to differences in population growth rates. Moreover, few demographic studies accounting for environmental stochasticity have been carried out both at continental and regional scales. In this study we calculated stochastic growth rates in five central and six northern peripheral populations of the widespread short-lived herb Plantago coronopus along the Atlantic Coast in Europe. To evaluate at two spatial scales how mean values and variability of vital rates (i.e. fecundity, recruitment, survival, growth and shrinkage) contributed to the differences in stochastic growth rates, we performed Stochastic Life Table Response Experiment analyses between and within central and peripheral regions. Additionally, we searched for correlations between vital rate contributions and local environmental conditions. Lower mean values and greater variability for some vital rates in peripheral than in central populations had an overall negative but non-significant effect on the stochastic growth rates in the periphery. Different life cycle components accounted for differences in population growth depending on spatial scale, although recruitment was the vital rate with the highest influence both between and within regions. Interestingly, the same pattern of differentiation among populations was found within central and peripheral areas: in both regions, one group of populations displayed positive contributions of growth and shrinkage and negative contributions of recruitment and survival, the opposite pattern being found in the remaining populations. These differences among populations within regions in vital rate contributions were correlated with precipitation regime, whereas at the continental scale, differences in contribution patterns were related to temperature. Altogether, our results show how populations of P. coronopus exhibit life cycle differences that may enable it to persist in locations with widely varying environmental conditions. This demographic flexibility may help to explain the success of widespread plants across large and heterogeneous ranges.We are grateful to M. Pazos for statistical assistance, to R. Braza for data of population F, to M. Maestro for soil analyses and to A. Adsuar, A. Barcos, R. Castillo, R. Corrià, J. Ehrlén, R. Forrest, A. de Frutos, E. López, J. Martínez, E. Morán, C. Niklasson, F. Ojeda, J. M. Olesen, S. Palacio, I. Pardolainen, A. Pérez, C. Pérez, P. Sánchez, A. Taboada, M. Talavera and A. Vale for helping in field and laboratory work. We also thank M. Franco and two anonymous reviewers for helpful comments on the 515 manuscript. The Spanish Ministry of Science and Innovation funded this research with two National Projects (CGL2006-08507; CGL2010-21642) to M.B.G. and a FPU grant to J.V.Peer reviewe

Divergence between phenotypic and genetic variation within populations of a common herb across Europe

Analyzing the pattern and causes of phenotypic and genetic variation within and among populations might help to understand life history variability in plants, and to predict their responses to changing environmental conditions. Here we compare phenotypic variation and genetic diversity of the widespread herb Plantago coronopus across Europe, and evaluate their relationship with environmental and geographical factors. Genetic diversity was estimated in 18 populations from molecular markers with AFLP. Phenotypic variation was measured in a subset of 11 populations on six life history traits (plant size, plant growth, fecundity, seed mass, mucilage production and ratio between two functionally different seed morphs). To account for ecological and geographical correlates, we estimated variability in local temperature, precipitation and intraspecific competition, and accounted for the central vs. peripheral position of populations. Phenotypic variation and genetic diversity were not significantly correlated within populations throughout the species' range. Phenotypic variation was positively linked to precipitation variability, whereas genetic diversity was correlated with the position of populations, suggesting that both types of variation are shaped by different processes. Precipitation seems to have acted as a selective agent for variation within populations in most life history traits, whereas the species' post-glacial demographic history has likely reduced genetic diversity in northern peripheral populations with respect to central ones. The positive association between precipitation variability and phenotypic variation also suggests that plant populations may have higher adaptive potential in ecologically variable rather than stable environments. Our study offers an additional criterion when predicting the future performance of species under environmental changes. © 2014 Villellas et al. - Copyright by the Ecological Society of AmericaThis study was funded by the Spanish Ministry of Science and Innovation by means of National Projects to M.B.G. (CGL2006-08507; CGL2010-21642) and A.T. (CGL2009-08713), and a FPU scholarship to J.V. We are grateful to A. Adsuar, A. Barcos, R. Braza, R. Castillo, M.L. Dehesa, R. Corrià, F. Domínguez, R. Forrest, M.C. García, E. López, J. Martínez, E. Morán, C. Niklasson, F. Ojeda, J.M. Olesen, S. Palacio, I. Pardo, A. Pérez, A. Primilla, C. Pérez, P. Sánchez, A. Taboada, M. Talavera and A. Vale for their valuable help in field and laboratory work through years. We thank R. Braza, V. Simón, J. Thompson and A. Traveset for plant material for genetic analyses, R. Braza for phenotypic data from population F and BN, and M. Pazos for her assessment in statistical analyses. X. Picó, J. Arroyo, T. Iriondo, P. Vargas and three anonymous referees provided very helpful comments on the manuscript.Peer Reviewe

The role of the tolerance-fecundity trade-off in maintaining intraspecific seed trait variation in a widespread dimorphic herb

Coexistence of species with different seed sizes is a long-standing issue in community ecology, and a trade-off between fecundity and stress tolerance has been proposed to explain co-occurrence in heterogeneous environments. Here we tested an intraspecific extension of this model: whether such trade-off also explains seed trait variation among populations of widespread plants under stress gradients. We collected seeds from 14 populations of Plantago coronopus along the Atlantic coast in North Africa and Europe. This herb presents seed dimorphism, producing large basal seeds with a mucilaginous coat that facilitates water absorption (more stress tolerant), and small apical seeds without coats (less stress tolerant). We analysed variation among populations in number, size and mucilage production of basal and apical seeds, and searched for relationships between local environment and plant size. Populations under higher stress (higher temperature, lower precipitation, lower soil organic matter) had fewer seeds per fruit, higher predominance of basal relative to apical seeds, and larger basal seeds with thicker mucilaginous coats. These results strongly suggest a trade-off between tolerance and fecundity at the fruit level underpins variation in seed traits among P. coronopus populations. However, seed production per plant showed the opposite pattern to seed production per fruit, and seemed related to plant size and other life-cycle components, as an additional strategy to cope with environmental variation across the range. The tolerance-fecundity model may constitute, under stress gradients, a broader ecological framework to explain trait variation than the classical seed size-number compromise, although several fecundity levels and traits should be considered to understand the diverse strategies of widespread plants to maximise fitness in each set of local conditions. © 2013. [The definitive version is available at www3.interscience.wiley.com]This study was funded by the Spanish Ministry of Science and Innovation through two National Projects (CGL2006-08507; CGL2010-21642) to M.B.G. and a scholarship (FPU) to J.V. We would like to thank R. Ajbilou, J. Ehrlén and J. M. Olesen for climate data, R. Braza and F. Ojeda for seed material from France and Morocco, M. Maestro for soil analyses, M. Pazos for valuable help in statistical analyses and S. Vicente for guidance in calculating evapotranspiration. We are also indebted to A. Adsuar, M. L. Dehesa, C. Pérez and A. Taboada for help with seed measurements. Two anonymous reviewers improved an earlier version of the manuscript.Peer Reviewe

Weak relationship between neutral genetic diversity and demography in a plant at continental scale

[ES] El comportamiento demográfico de las poblaciones resulta determinante para la abundancia y distribución de las especies, por lo que identificar las causas de su variación permite una mejor gestión de la biodiversidad. Además del efecto de las condiciones ambientales, la diversidad genética puede tener consecuencias demográficas importantes, pero existe un mayor conocimiento de tales efectos en especies amenazadas que en organismos comunes. En el presente estudio se analizaron los efectos de las condiciones ambientales en la demografía de una planta de amplia distribución, Plantago coronopus, a lo largo de su rango latitudinal europeo, considerando las diferencias en diversidad genética neutral. La diversidad genética sólo mostró relación con uno de los parámetros demográficos analizados, el crecimiento individual, y no mostró ninguna influencia sobre la tasa de crecimiento poblacional. En cambio, diversos factores ambientales abióticos (clima, suelo) y bióticos (densidad poblacional) tuvieron una mayor influencia en los componentes del ciclo vital (supervivencia, crecimiento, reproducción). Estas tasas individuales presentaron respuestas opuestas entre ellas a los factores ambientales, fenómeno conocido como compensación demográfica, lo que resultó en una ausencia de patrón en la tasa de crecimiento poblacional a lo largo del gradiente ambiental. Estos resultados destacan la importancia de considerar múltiples parámetros demográficos individuales y poblacionales para evaluar de manera consistente la relación entre genética, condiciones ambientales y demografía en una especie. Nuestro estudio también sugiere que, en especies de distribución amplia, los factores genéticos pueden resultar menos útiles que las variables ambientales para predecir su comportamiento y futura distribución ante nuevos escenarios ecológicos.[EN] Population performance is determinant for the abundance and distribution of species and identifying the causes of its variation allows a better management of biodiversity. Besides the effect of environmental conditions, genetic diversity may also have significant demographic consequences, but there is greater knowledge of such effects in threatened species than in common organisms. In the present study, the influence of environmental conditions on the demography of a widespread herbaceous plant, Plantago coronopus, was analyzed throughout its European latitudinal range, considering also differences in neutral genetic diversity. Genetic diversity was only related to one of the demographic parameters analyzed, individual growth, and showed no influence on the population growth rate. In contrast, several abiotic (climate, soil) and biotic (population density) environmental factors had a greater influence on the life cycle components (survival, growth, reproduction). These individual rates showed opposite responses to environmental factors, a phenomenon known as demographic compensation, which resulted in an absence of pattern in the population growth rate along the environmental gradient. Our results highlight the importance of considering multiple individual and population demographic parameters to evaluate the relationship between a species genetics, environmental conditions, and demography. This study also suggests that, in organisms with wider distribution ranges, genetic factors may be less useful than environmental variables to predict population trends and future distribution in new ecological scenarios.Este trabajo fue financiado por el Ministerio de Ciencia e Innovación mediante dos Proyectos Nacionales (CGL2006-08507; CGL2010-21642) a M.B.G, y una beca de doctorado FPU a J.V