Collective behavior of biological aggregates

Mención Internacional en el título de doctorThe behavior of living systems can exhibit emergent phenomena that are not present in their individual components. Living systems are far from equilibrium, may lack conservation laws and using tools from statistical physics and thermodynamics is challenging. However, quantitative observations and experiments yield a wealth of data that allow to design models capturing important aspects of the behavior of these systems. This thesis focuses on two topics, the collective behavior of midge swarms and the collective behavior of bacterial biofilms. Prior studies of insect swarms have focused on their formation as an ordering phase transition, which fails to capture many qualitative and quantitative features. In this thesis we study the Vicsek model confined by a harmonic potential. By using dynamical systems and statistical mechanics tools, we have discovered a novel phase transition characterized by scale free chaos, which exhibits power laws and present qualitative features compatible with observations of swarms of male midges in nature and in the laboratory. On the second topic, bacterial biofilms pose a challenge to theorists, who must model elements on different spatial and temporal scales. We present a hybrid model based on an architecture of immersed boundaries with a dynamic energy budget metabolism. The model captures geometric differences between bacteria, being able to reproduce varied patterns depending on their shapes and competence phenomena between different types. We can study antibiotic resistance in biofilms and test cocktails to eradicate them.El comportamiento de los sistemas vivos puede mostrar fenómenos emergentes que no están presentes en sus componentes individuales. Los sistemas vivos están alejados del equilibrio, pueden carecer de leyes de conservación y es todo un reto emplear herramientas de la física estadística y la termodinámica. Experimentos y observaciones cuantitativas producen una gran cantidad de datos que permiten diseñar modelos que expliquen aspectos importantes del comporamiento de estos sistemas. Esta tesis se centra en dos temas, el comportamiento colectivo de los enjambres de insectos voladores como los mosquitos y el comportamiento colectivo de las biopelículas bacterianas. Los estudios previos de enjambres de insectos se han centrado en su formación como una transición orden-desorden, lo que no explica muchos aspectos tanto cualitativos como cuantitativos. En esta tesis estudiamos el modelo de Vicsek confinado por un potencial armónico. Usando herramientas de sistemas dinámicos y de mecánica estadística hemos descubierto una nueva transición de fase caracterizada por caos libre de escalas, que presenta leyes de potencias y tiene rasgos cualitativos compatibles con las observaciones y experimentos de laboratorio de enjambres de dípteros. Por otro lado, las biopelículas bacterianas plantean un reto teórico, pues se debe modelar elementos a diferentes escalas espaciales y temporales. Presentamos un modelo híbrido basado en una arquitectura de fronteras inmersas con un metabolismo de presupuesto de balance energético. El modelo captura las diferencias geométricas entre bacterias, generando patrones diversos según su forma y competencia entre bacterias de distintos tipos. Permite estudiar la resistencia de biopelículas a antibióticos y el diseño de cócteles para erradicarlos.Agradezco el apoyo del Ministerio de Economía y Competitividad de España a través de las ayudas del programa de Formación de Doctores, PRE2018-083807, cofinanciada por el Fondo Social Europeo. También agradezco al apoyo de FEDER /Ministerio de Ciencia, Innovación y Universidades - Agencia Estatal de Investigación por medio de los proyectos MTM2017-84446-C2-1-R y PID2020-112796RB-C21.Programa de Doctorado en Ingeniería Matemática por la Universidad Carlos III de MadridPresidente: Björn Birnir.- Secretaria: Ester Aurora Torrente Orihuela.- Vocal: Antonio Prados Montañ

High Correlated Paternity Leads to Negative Effects on Progeny Performance in Two Mediterranean Shrub Species

Anthropogenic habitat deterioration can promote changes in plant mating systems that subsequently may affect progeny performance, thereby conditioning plant recruitment for the next generation. However, very few studies yet tested mating system parameters other than outcrossing rates; and the direct effects of the genetic diversity of the pollen received by maternal plants (i.e. correlated paternity) has often been overlooked. In this study, we investigated the relation between correlated paternity and progeny performance in two common Mediterranean shrubs, Myrtus communis and Pistacia lentiscus. To do so, we collected open-pollinated progeny from selected maternal plants, calculated mating system parameters using microsatellite genotyping and conducted sowing experiments under greenhouse and field conditions. Our results showed that some progeny fitness components were negatively affected by the high correlated paternity of maternal plants. In Myrtus communis, high correlated paternity had a negative effect on the proportion and timing of seedling emergence in the natural field conditions and in the greenhouse sowing experiment, respectively. In Pistacia lentiscus, seedling emergence time under field conditions was also negatively influenced by high correlated paternity and a progeny survival analysis in the field experiment showed greater mortality of seedlings from maternal plants with high correlated paternity. Overall, we found effects of correlated paternity on the progeny performance of Myrtus communis, a self-compatible species. Further, we also detected effects of correlated paternity on the progeny emergence time and survival in Pistacia lentiscus, an obligate outcrossed species. This study represents one of the few existing empirical examples which highlight the influence that correlated paternity may exert on progeny performance in multiple stages during early seedling growth.España , Ministerio de Ciencia e Innovación CGL2008-00938 and CGL2011-23721

Extensive pollen flow but few pollen donors and high reproductive variance in an extremely fragmented landscape

Analysing pollen movement is a key to understanding the reproductive system of plant species and how it is influenced by the spatial distribution of potential mating partners in fragmented populations. Here we infer parameters related to levels of pollen movement and diversity of the effective pollen cloud for the wind-pollinated shrub Pistacia lentiscus across a highly disturbed landscape using microsatellite loci. Paternity analysis and the indirect KinDist and Mixed Effect Mating models were used to assess mating patterns, the pollen dispersal kernel, the effective number of males (N(ep)) and their relative individual fertility, as well as the existence of fine-scale spatial genetic structure in adult plants. All methods showed extensive pollen movement, with high rates of pollen flow from outside the study site (up to 73-93%), fat-tailed dispersal kernels and large average pollination distances (δ = 229-412 m). However, they also agreed in detecting very few pollen donors (N(ep) = 4.3-10.2) and a large variance in their reproductive success: 70% of males did not sire any offspring among the studied female plants and 5.5% of males were responsible for 50% of pollinations. Although we did not find reduced levels of genetic diversity, the adult population showed high levels of biparental inbreeding (14%) and strong spatial genetic structure (S(p) = 0.012), probably due to restricted seed dispersal and scarce safe sites for recruitment. Overall, limited seed dispersal and the scarcity of successful pollen donors can be contributing to generate local pedigrees and to increase inbreeding, the prelude of genetic impoverishment

A phylogenetic hypothesis for Helianthemum (Cistaceae) in the Iberian Peninsula

We have sequenced the nuclear DNA internal transcribed spacer (ITS1+5.8S+ITS2) from samples collected in the field belonging to all taxa of Helianthemum in the Iberian Peninsula and analysed the data matrix by both Bayesian and Maximum Likelihood approaches. The phylogenetic hypothesis that we present here provides strong support for the monophyly of the genus and for the above-species systematics (sections and subgenera) considered in Flora iberica. Nevertheless, most species and subspecies in sections Helianthemum and Pseudocistus clustered in ample polytomies with poor resolution and branch support. This topology is interpreted to be consequence of frequent events of hybridization and introgression and/or rapid adaptive radiation in the genus Helianthemum, the most diversified lineage within the family Cistaceae.En este trabajo presentamos una hipótesis filogenética para el género Helianthemum en la Península Ibérica. Para ello hemos recolectado en el campo material de todos los taxones y analizado las secuencias del marcador nuclear ITS (internal transcribed spacer) completo (ITS1+5.8S+ITS2) tanto con métodos Bayesianos como de Máxima Verosimilitud. Nuestra hipótesis muestra gran apoyo para la monofilia de género y para los taxones supra-específicos considerados en Flora iberica (secciones y subgéneros). En cambio, las especies y subespecies de las secciones más extensas (Helianthemum y Pseudocistus) se han agrupado en amplias politomías con muy bajo apoyo. Interpretamos que esta marcador nuclear tiene baja resolución debido a eventos frecuentes de hibridación e introgresión así como de radiación adaptativa en el género Helianthemum, que es el linaje más diversificado de toda la familia Cistaceae

Genetic structure and population differentiation of the Mediterranean pioneer spiny broom Calicotome villosa across the Strait of Gibraltar

The region around the Strait of Gibraltar is considered to be one of the most relevant 'hot spots' of biodiversity in the Mediterranean Basin due to its historical, biogeographical, and ecological features. Prominent among these is its role as a land bridge for the migration and differentiation of species during the Pleistocene, as a consequence of the lowering of sea level and climate changes associated with the Ice Ages. In the present study, we report a multilevel hierarchical investigation of the genetic diversity of Calicotome villosa, a common pioneer legume shrub, at the regional scale. The results of genetic analysis of progeny arrays are consistent with a predominantly outcrossing mating system in all the populations analysed. Geographically, a pattern of population isolation by distance was found, but the Strait accounted for only approximately 2% of the among-population genetic differentiation. Consequently, extensive historical gene flow appears to be the rule for this species in this area. According to the natural history traits of C. villosa (pollination, dispersal, and colonization ability), we hypothesize that gene flow must be strongly influenced by seed dispersal because pollen flow is very limited. Based on the history of trade and land use, cattle and human movements across the Strait must have strongly favoured seed dispersal. We review and discuss these results and compare them with those of other reported studies of genetic and phylogenetic differentiation across the Strait of Gibraltar. It is stressed that colonization ability, which depends upon seed dispersal and life form, can be a more critical factor in gene flow than pollination.Junta de Andalucía PB0551-95, PB1144-98BOS, 2003-07924-CO2-01 to J.A

Revisión de la biología reproductiva de Pistacia lentiscus (Anacardiaceae): una especie clave Mediterránea en el Antropoceno

El lentisco (Pistacia lentiscus L., Anacardiaceae) es uno de los arbustos más abundantes y característicos de la cuenca Mediterránea. Sus frutos, tipo drupa, son el principal reclamo y fuente alimenticia de los frugívoros invernantes de esta región estableciendo una interacción muy importante planta-animal, pero el cambio del uso del suelo y la poca cobertura natural que queda en la región pueden poner en peligro esta interacción planta animal y el futuro de las poblaciones de lentiscos. Aunque existen numerosos estudios sobre la biología reproductiva de esta planta es necesario enmarcar estos conocimientos en un contexto de fragmentación del hábitat. La presión antropogénica extrema puede llegar a aislar físicamente los fragmentos y restringir los microhábitats seguros dentro de los bosques. Al aumentar el aislamiento, no solo la nube de polen disponible para las plantas femeninas es menos diversa, sino que además la abundancia de dispersores presentes es menor, modificando el destino final de las semillas. A nivel genético, es frecuente la existencia de cuellos de botella en las poblaciones de adultos, pero no se ve el efecto tan marcado de estructuración genética como en otras especies de matorral Mediterráneo. Este trabajo revisa el conocimiento existente sobre la biología reproductiva del lentisco en el contexto actual de cambio global y antropización del paisaje, con el fin de predecir posibles escenarios futuros y asegurar la viabilidad de esta especie.The mastic tree (Pistacia lentiscus L., Anacardiaceae) is one of the most abundant and characteristic shrubs in the Mediterranean basin. Its fruits, drupe type, are the main claim and food source of the wintering frugivores of this region establishing a very important plant-animal interaction, but the past and current change in land use and the little natural cover that remains in the region may endanger this interaction between animals and plant and the future of mastic tree populations. Although there are numerous studies on the reproductive biology of this plant it is necessary to frame this knowledge in a context of habitat fragmentation. Extreme anthropogenic pressure can physically isolate the fragments and restrict safe microhabitats within forests for seeds to grow. By increasing the isolation, not only is the pollen cloud available to female plants less diverse, but also the abundance of dispersers is lower modifying the final destination of the seeds. Population bottlenecks are frequent in the populations of adult plants, but the effect of genetic structuring is not as evident as in other Mediterranean shrub species. This paper reviews existing knowledge on reproductive biology of P. lentiscus in the current context of global change and human impact on the landscape, in order to predict possible future scenarios and ensure the viability of this species

Maximize Resolution or Minimize Error? Using Genotyping-By-Sequencing to Investigate the Recent Diversification of Helianthemum (Cistaceae)

A robust phylogenetic framework, in terms of extensive geographical and taxonomic sampling, well-resolved species relationships and high certainty of tree topologies and branch length estimations, is critical in the study of macroevolutionary patterns. Whereas Sanger sequencing-based methods usually recover insufficient phylogenetic signal, especially in recently diversified lineages, reduced-representation sequencing methods tend to provide well-supported phylogenetic relationships, but usually entail remarkable bioinformatic challenges due to the inherent trade-off between the number of SNPs and the magnitude of associated error rates. The genus Helianthemum (Cistaceae) is a species-rich and taxonomically complex Palearctic group of plants that diversified mainly since the Upper Miocene. It is a challenging case study since previous attempts using Sanger sequencing were unable to resolve the intrageneric phylogenetic relationships. Aiming to obtain a robust phylogenetic reconstruction based on genotyping-by-sequencing (GBS), we established a rigorous methodological workflow in which we i) explored how variable settings during dataset assembly have an impact on error rates and on the degree of resolution under concatenation and coalescent approaches, ii) assessed the effect of two extreme parameter configurations (minimizing error rates vs. maximizing phylogenetic resolution) on tree topology and branch lengths, and iii) evaluated the effects of these two configurations on estimates of divergence times and diversification rates. Our analyses produced highly supported topologically congruent phylogenetic trees for both configurations. However, minimizing error rates did produce more reliable branch lengths, critically affecting the accuracy of downstream analyses (i.e. divergence times and diversification rates). In addition to recommending a revision of intrageneric systematics, our results enabled us to identify three highly diversified lineages in Helianthemum in contrasting geographical areas and ecological conditions, which started radiating in the Upper Miocene.España, MINECO grants CGL2014- 52459-P and CGL2017-82465-PEspaña, Ministerio de Economía, Industria y Competitividad, reference IJCI-2015-2345

Una aproximación a la ecología epigenética en plantas

El estudio de la epigenética, cambios químicos estables que no suponen cambios en la secuencia de nucleótidos, ha avanzado considerablemente en los últimos años. Estos cambios son modulables por el ambiente, y pueden ser heredados por las generaciones siguientes. Hay una creciente evidencia de que la variación hereditaria en los rasgos ecológicamente relevantes se puede generar a través de un conjunto de mecanismos epigenéticos, incluso en ausencia de variación genética. Desde un punto de vista evolutivo, la variabilidad generada por mecanismos epigenéticos amplía la variabilidad de fenotipos al aparecer nuevos epialelos que pueden ser seleccionados en poblaciones naturales, reflejando la idea de que la herencia puede no ser tan rígida. Por medio de la regulación epigenética se puede observar cómo es la adaptación al medio ambiente dada por la plasticidad del genoma, la cual tiene como resultado la formación de distintos fenotipos según el medio ambiente al que sea expuesto el organismo. A pesar de la importancia de estos mecanismos aún hay pocos trabajos experimentales que desentrañen las preguntas básicas de ecología epigenética y menos aun los que se han centrado en plantas no modelo.The study of epigenetics, stable chemical changes that do not involve changes in the sequence of nucleotides, has greatly advanced in recent years. These changes can be shaped by the environment and can be inherited into the following generations. There is growing evidence that the inherited variation in ecologically relevant traits can be generated through a set of epigenetic mechanisms, even in the absence of genetic variation. From an evolutionary point of view, the variability generated by epigenetic mechanisms increases the variability of phenotypes when new epialleles appear that can be selected in natural populations, reflecting the idea that inheritance might be not so inflexible. By means of epigenetic regulation it can be observed how adaptation to the environment is given by the plasticity of the genome, which results in the formation of different phenotypes according to the environment to which the organism is exposed. Despite the importance of these mechanisms there are still few experimental studies that unravel the basic questions of epigenetic ecology and even less those that have focused on non-model plant species.Plan Nacional del Ministerio Economía y Competitividad de España CGL2011-23721Beca del Ministerio de Economía y Competitividad de España BES-2012-055103Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET)Universidad Nacional de Córdoba (Argentina

The role of plant–pollinator interactions in structuring nectar microbial communities

Floral nectar harbours a diverse microbiome of yeasts and bacteria that depend predominantly on animal visitors for their dispersal. Since pollinators visit specific sets of flowers and carry their own unique microbiota, we hypothesize that plant species visited by the same set of pollinators may support non-random nectar microbial communities linked together by the type of pollinator. Here we explore the importance of plant–pollinator interactions in the assembly of nectar microbiome and study the role of plant geographic location as a determinant of microbial community composition. We intensively sampled the nectar of 282 flowers of 48 plant species with beetles, birds, long-tongued and short-tongued insects as pollinators in wild populations in South Africa, one of the world's biodiversity hotspots, and using molecular techniques we identified nectar yeast and bacteria taxa. The analyses provided new insights into the richness, geographic structure and phylogenetic characterization of nectar microbiome, and compared patterns of composition of bacteria and yeast communities in relation to plant and pollinator guild. Our results showed that plant–pollinator interactions played a crucial role in shaping nectar microbial communities. Plants visited by different pollinator guilds supported significantly different yeast and bacterial communities. The pollinator guild also contributed to the maintenance of beta diversity and phylogenetic microbial segregation. The results revealed different patterns for yeast and bacteria; whereas plants visited by beetles supported the highest richness and phylogenetic diversity of yeasts, bacteria communities were significantly more diverse in plants visited by other insect groups. We found no clear microbial spatial segregation at different geographical scales for bacteria, and only the phylogenetic similarity of yeast composition was correlated significantly with geography. Synthesis. Interactions of animal vector, plant host traits and microbe physiology contribute to microbial community assemblages in nectar. Our results suggest that plants visited by the same pollinator guild have a characteristic nectar microbiota signature that may transcends the geographic region they are in. Contrasted patterns for yeast and bacteria stress the need for future work aimed at better understanding the causes and consequences of the importance of plants and pollinators in shaping nectar microbial communities in nature.Ministerio de Economía y Competitividad SEV-2012- 0262Ministerio de Ciencia e Innovación RYC2018-023847-