Modeling the Genetic Consequences of Mutualism on Communities

Three models of coevolutionary dynamics between mutualistically interacting species are developed. The first is a three loci, haploid model describing a general plant-pollinator system, such as Greya moth and its host plant. In this case, the system will always collapse to a single plant type and pollinator type. In a community with an mutant plant type, it is possible for a host-switch to occur, governed by the initial relative abundance plant type and the pollinator choosiness. In addition, genetic diversity can be maintained if the pollinator has no differential host preference, only adaptation to a host. Next, this model is extended to the case of the fig-fig wasp system, implementing a more complex life cycle of overlapping generations due to asynchronous flowering populations. In the fig system, extensive hybridization due to asynchronous flowering can maintain genetic diversity for thousands of generations, when pollinator choosiness is high. Therefore, mutualism can lead to low confidence trees in phylogenetic reconstructions affecting discordance among plant and pollinator phylogenetic trees. Lastly, the consequences of host-switching and other speciation events on coevolving phylogenies are explored through stochastic numerical simulations. The goal is to determine to what extent cophylogeny should be expected between mutualistic partners and what features of mutualistic webs can be explained by mutualistic coevolution alone

Tritrophic interactions among plants, herbivores and plant mutualists

Plants form the first trophic level in terrestrial ecosystems and provide energy and nutrients to higher trophic levels. Herbivores, frugivores or fungal endophytes use plants directly, while predators consume plants indirectly by consuming herbivores. However, species are often simultaneously interacting with antagonistic and mutualistic partners at various trophic levels. For this reason, the outcomes of species interactions can indirectly affect other species in the community. The aim of my thesis was to study tritrophic interactions between plants, their antagonists, such as insect or avian herbivores, and mutualists such as insectivorous or frugivorous birds and symbiotic endophyte fungus. In Chapters I-III I concentrated on the interactions among plants, herbivores and protective plant mutualists. In the first two Chapters, I investigated whether birds use volatile organic compounds or changes in visual properties of leaves from herbivore-damaged trees as foraging cues. I found that trees respond to herbivore damage both locally and systemically, but the olfactory foraging cue hypothesis was not supported. Instead, herbivory affected visual properties of leaves viewed by birds, although these changes may be in the limit of detection to them. In addition, my results indicate that cryptically coloured herbivores may have slightly better camouflage when on herbivore-damaged trees, although the herbivores are discriminable to birds against the leaves of the host plant regardless of the treatment (Chapter II). In Chapter III I studied the relationship between plants and protective fungal symbiont by testing whether systemic endophyte fungi can protect grasses against wild avian grazers. In this study I used two grass species, red fescues and tall fescues, which differ in texture. Both species have naturally both endophytic and non-endophytic individuals. I found that softer red fescue was preferred over coarse tall fescue, regardless of the endophyte status. In Chapter IV I studied the interaction between plants, herbivores and seed-dispersing mutualists. I tested whether insect herbivory causes allocation cost to fleshy fruiting plants by affecting ripening or chemical composition of berries. I also investigated potential ecological cost of herbivory measured as probability for ripe berries to be removed by frugivorous birds. I found that berries in undamaged ramets neighbouring herbivore-damaged conspecifics had lower probability to be removed by frugivores, although herbivory did not affect ripening or chemical composition of berries. This indicates that in clonal plants, herbivore damage may cause priming effect on neighbouring ramets, which can affect plant mutualists. The results of this thesis extend current knowledge about plant responses to herbivory, and also how these responses affect plant mutualists. In addition, my thesis provides information about the foraging behaviour of herbivores and plant mutualists. This kind of knowledge is essential for biological control and agricultural procedures, as well as on the planning of urban grass areas.Kasvit muodostavat ensimmäisen ravintoketjun tason eli trofiatason maaekosysteemeissä, ja näin ollen toimivat ravinnon ja energianlähteinä ylemmille trofiatasoille. Kasvinsyöjät eli herbivorit, hedelmänsyöjät eli frugivorit ja symbionttiset endofyyttisienet ovat suoraan riippuvaisia kasveista, kun taas herbivoreja syövien petojen riippuvuus kasveista on epäsuoraa. Eri trofiatasoilla olevat lajit ovatkin jatkuvassa vuorovaikutuksessa keskenään, minkä vuoksi kahden lajin väliset vuorovaikutussuhteet voivat vaikuttaa myös muihin lajeihin. Väitöskirjassani olen tarkastellut usean trofiatason välisiä yhteyksiä kasvien ja niille haitallisten ja hyödyllisten eliöiden, eli antagonistien ja mutualistien, välillä. Esimerkkeinä antagonisteista käytin hyönteis- ja lintuherbivoreja, kun taas mutualisteina käytin hyönteissyöjälintuja, endofyyttisieniä ja siementenlevittäjälintuja. Tutkimuksissa I-II tutkin herbivorian aiheuttamien kasvista haihtuvien yhdisteiden, ja lehdissä tapahtuvien visuaalisten muutosten vaikutusta hyönteissyöjälintujen ravinnonhankintakäyttäytymiseen. Kasvit reagoivat sekä paikallisesti että kokonaisvaltaisesti herbivorian aiheuttamiin vaurioihin. En kuitenkaan löytänyt selvää tukea sille, että haihtuvat yhdisteet toimisivat hajuvihjeinä linnuille. Sen sijaan sain selville, että kasvinsyöjien aiheuttamat vauriot voivat vaikuttaa kasvin vahingoittumattomien lehtien ulkonäköön, joskin nämä muutokset voivat olla lintujen visuaalisen erotuskyvyn rajoilla. Herbivorian aiheuttamat muutokset kasvissa voivat lisäksi tehdä kryptisestä herbivorista vähemmän näkyvän linnuille, vaikka linnut todennäköisesti erottavatkin herbivorin lehtiä vasten riippumatta siitä onko kasvia vahingoitettu vai ei (II). Tutkimuksessa III tutkin voivatko endofyyttisienet suojella heiniä hanhien laidunnukselta. Tässä tutkimuksessa käytin kahta heinälajia, jotka eroat karkeudeltaan. Molemmilla lajeilla osa yksilöistä oli luontaisesti endofyytillisiä ja osa endofyytittömiä. Tulokseni osoittavat, että hanhet suosivat pehmeämpää ruoholajia karkean ruohon sijaan riippumatta endofyyttisienen läsnäolosta. Tutkimuksessa IV testasin aiheuttaako hyönteisherbivoria allokaatiokustannuksia kasville vaikuttamalla marjojen kypsymiseen tai biokemialliseen koostumukseen. Tutkin myös mahdollisia herbivorian aiheuttamia ekologisia kustannuksia kasville, joita mittasin marjojen todennäköisyytenä tulla siementenlevittäjien syömiksi. Tulokseni osoittavat, että marjoilla, jotka kasvoivat varvuissa lähellä herbivorien vaurioittamia varpuja, oli pienempi todennäköisyys tulla siementenlevittäjien syömiksi. Herbivoria ei vaikuttanut marjojen kypsymiseen tai biokemialliseen koostumukseen. Tämä viittaa siihen, että klonaalisilla kasveilla herbivoria voi aiheuttaa puolustusreaktion vahingoittumattomissa naapurikasveissa, mikä voi vaikuttaa myös kasvien mutualisteihin. Tämän väitöskirjan tutkimukset syventävät ymmärrystämme siitä, miten kasvit reagoivat herbivoriaan, ja miten nämä reaktiot vaikuttavat kasvien mutualisteihin. Tutkimukseni lisäävät myös tietoa herbivorien ja kasvien mutualistien ravinnonhankintakäyttäymisestä. Tällainen tieto on oleellista niin biologisen torjunnan kuin maataloudenkin kannalta, ja sitä voidaan soveltaa myös viheralueiden suunnittelussa.Siirretty Doriast

Natural and human-induced dynamics in plant–animal mutualistic networks

Species interactions are an integral part of ecological communities. Collectively, these interactions form complex and highly dynamic networks. The structure of these networks varies due to geographic and temporal variation in the abundance and co-occurrence of interacting species and due to species gains and losses after anthropogenic perturbation. In Europe’s last relict of old-growth lowland forest (Białowieża, Poland), I studied the outcomes of these natural and human-induced dynamics in highly diversified mutualistic networks of plants, pollinators and seed dispersers. These mutualistic interactions between plants and free-living animals are of great importance, as the flowers and fruits of many plant species are critical resources for a variety of animal species, which in turn contribute significantly to the regeneration of plant communities. As part of my studies, I was able to show that plant–animal mutualistic networks are highly dynamic systems that respond collectively to changing biotic context and human-induced perturbation. Observed shifts in facilitative and competitive interactions among plants sharing mutualistic partners show that biotic context is a strong determinant of the outcome of interspecific interactions. The use of network analyses, thereby, allowed me to identify some of the mechanisms that shape species interactions and their outcomes. For example, my studies show that a change in the population density of one species suffices to trigger cascading effects on the interactions and populations of other species. This finding highlights that species interactions may have a pervasive effect on the assembly and disassembly of ecological communities. Even more importantly, I could show that these community-wide dynamics were in all cases linked to consumer-resource relationships, which are key determinants of plant–animal mutualisms. Thus, changes in the foraging behaviour of animals in response to variation in the density of plant resources and competitors affected the structure of mutualistic communities. This underscores that despite the evolutionary conservatism in ecological interactions, biotic context determines to which extent these coevolved interactions are realized. The fact that the sharing of mutualistic partners among plant species was reflected in their co-occurrence demonstrates that the above-mentioned dynamics in ecological networks may also determine community assembly processes and species co-existence. Importantly, the comparison of several types of species interactions revealed how biotic context in its various forms can shape land-use effects on species interactions. I found that the mutualism between plants and seed dispersers was more susceptible to habitat degradation than the mutualism between plants and their pollinators. This finding highlights that a high degree of generalization, such as in the seed dispersal mutualism, does not necessarily buffer ecological communities against the loss of species. This becomes even more important if a few species have a disproportionate effect on a given target function and if species are particularly vulnerable to ecological perturbation, such as habitat specialists or large-bodied frugivores. Furthermore, I observed that shifts in the abundance of plant resources in degraded habitats can amplify land-use effects on plant–animal mutualistic interactions. Importantly, changes in the density of plant resources explained about 40 to 70 percent of the variation in land-use effects on interactions between plants and their pollinators and seed dispersers. This demonstrates that a consideration of biotic context (e.g. in the form of resources) may considerably improve predictions of the magnitude of land-use effects on species interactions. Thereby, the correlated responses of pollinators and seed dispersers to the shifts in plant population densities in degraded habitats highlight that these dynamics are not restricted to single types of interaction, but potentially operate at the level of ecosystems. Studies that only focus on subsets of species or interaction types may be unable to identify the consequences of human land-use that have been shown here. In principle, the results of the presented studies may also be valid for other types of mutualistic and antagonistic interactions that are based on consumer-resource relationships. Altogether, the results of my thesis suggest that natural and human-induced dynamics in plant–animal mutualistic networks follow similar principles. In the worst case these dynamics might have cascading effects on the functioning and integrity of ecosystems through a parallel loss of multiple animal-mediated ecosystem services after habitat degradation

Conflicting Selection in the Course of Adaptive Diversification: The Interplay between Mutualism and Intraspecific Competition

Adaptive speciation can occur when a population undergoes assortative mating and disruptive selection caused by frequency-dependent intraspecific competition. However, other interactions, such as mutualisms based on trait matching, may generate conflicting selective pressures that constrain species diversification. We used individual-based simulations to explore how different types of mutualism affect adaptive diversification. A magic trait was assumed to simultaneously mediate mate choice, intraspecific competition, and mutualisms. In scenarios of intimate, specialized mu- tualisms, individuals interact with one or few individual mutualistic partners, and diversification is constrained only if the mutualism is obligate. In other scenarios, increasing numbers of different partners per individual limit diversification by generating stabilizing selection. Stabilizing selection emerges from the greater likelihood of trait mismatches for rare, extreme phenotypes than for common intermediate phenotypes. Constraints on diversification imposed by increased numbers of partners decrease if the trait matching degree has smaller positive effects on fitness. These results hold after the relaxation of various assumptions. When trait matching matters, mutualism-generated stabilizing selection would thus often constrain diversification in obligate mutualisms, such as ant-myrmecophyte associations, and in low-intimacy mutualisms, including plant-seed disperser systems. Hence, different processes, such as trait convergence favoring the incorporation of nonrelated species, are needed to explain the higher richness of low-intimacy assemblages—shown here to be up to 1 order of magnitude richer than high-intimacy systems

Chemical Plant Defense Against Herbivores

Herbivores can damage plant productivity and fitness because plants have improved defense mechanisms such as physical barriers, association with other organisms such as ants, and chemical defense. In that, separate plant species produce different chemical molecules. Chemical compounds involved in plant defense can act in several facts: decreased palatability, like a poison, such as a stunner, and increased gene defense expression, among others. In this chapter, we approach several examples of chemical molecules produced by plants to defend themselves, including biochemical metabolic pathways, as well as ecological and evolutive implications

On the diversification of highly host-specific symbionts: the case of feather mites.

One of the most relevant and poorly understood topics in Evolutionary Ecology is symbiont evolutionary diversification. Since Fahrenholz's rule (1913), the idea of symbionts speciating following hosts speciation (i.e., cospeciating) has been pervasive. Recent studies, however, have shown that host-shift speciation (speciation after switching to a new host) is almost as relevant as cospeciation in explaining symbiont diversification. Also, these studies have revealed that methodological biases have favored cospeciation. Nonetheless, most symbiont groups, especially those highly host-specific and specialized in which cospeciation is expected to be the rule, such as the feather mites of birds, were yet to be studied. Symbionts are the most abundant and diverse organisms on Earth, and thus essential components of ecosystems. However, symbionts have attracted historically less attention than other organisms and their study entails numerous methodological challenges, so surprisingly little is understood about the basic biology and ecology of many symbiont groups, especially the non-parasitic. By studying vane-dwelling feather mites living permanently on the surface of flight feathers of birds (Acariformes: Astigmata: Analgoidea and Pterolichoidea), this thesis is a contribution to fill this gap. This thesis is divided into three parts: 1) First, resources and molecular tools enabling large-scale studies of feather mites are developed. 2) Then, these and other tools are used to investigate eco-evolutionary aspects relevant to understand feather mite diversification, such as their mode of transmission and the type of interaction they have with their hosts. 3) Finally, feather mites diversification at a macro- and microevolutionary scale is investigated. The first part compiles a global database of bird-feather mites associations. Also, it evaluates and adjusts DNA barcoding and metabarcoding to be suitable methodologies for studying feather mites. The second part reveals feather mites as highly specialist and hostspecific symbionts whose main mode of transmission is vertical. Analyses of feather mites diet reveal them as trophic generalists which maintain a commensalistic-mutualistic relationship with birds. Finally, the last part of the thesis shows host-shift speciation as the primary process driving the diversification of feather mites. Also, it highlights that majorhost switching, despite being an infrequent process, is highly relevant for the diversification of this group. Lastly, analyses of straggling reveal a high rate of preferential straggling governed by ecological filters. Overall, despite feather mites are revealed as highly specialized and host-specific symbionts, the coevolutionary scenario is highly dynamic. Straggling and host-switching are prevalent processes which allow colonizing new hosts in highly specialized and hostspecific symbionts. Accordingly, coevolution and codiversification do not operate in isolated host-symbiont interactions but more likely in a manner compatible with the geographic mosaic of coevolution. Finally, ecological fitting and interspecific competition are most likely the main factors governing the (co)eco-evolutionary dynamics.La diversificación evolutiva de los simbiontes es uno de los aspectos más relevantes, pero menos entendidos en Ecología Evolutiva. Desde la regla de Fahrenholz (1913), la idea de que los simbiontes especian a la par que sus hospedadores (i.e. coespecian) ha sido extremadamente popular. Sin embargo, estudios recientes han encontrado que la especiación por salto de hospedador (el proceso de especiación que ocurre cuando los simbiontes especian a consecuencia de un cambio de hospedador) es casi tan relevante como la coespeciación. Estos estudios, además, han encontrado que problemas metodológicos favorecían que se encontraran evidencias de coespeciación donde no las había. En cualquier caso, los procesos de diversificación evolutiva de la mayoría de los grupos de simbiontes nunca han sido investigados. Especialmente de aquellos altamente especializados y específicos en términos de hospedador, que son aquellos donde el proceso de coespeciación se espera que sea más relevante, como los ácaros de las plumas de las aves. Los organismos simbiontes son el grupo más abundante y diverso de la tierra, por ende, son componentes esenciales de los ecosistemas. Sin embargo, históricamente los simbiontes han atraído menos la atención de los investigadores, en parte debido a que su estudio conlleva numerosos retos metódologicos. De hecho, debido a esto, actualmente se desconoce una gran parte de aspectos sobre su biología básica y ecología, especialmente de aquellos simbiontes no parásitos. Ésta tésis pretende completar este vacío de conocimiento mediante el estudio de los ácaros de las plumas de las aves. La tésis está dividida en tres partes: 1) En la primera parte se han generado recursos y herramientas moleculares para estudios a gran escala en este grupo de simbiontes. 2) Despues, éstas y otras herramientas se han usado para investigar aspectos eco-evolutivos relavantes para entender el proceso de diversificación evolutiva, tales como, el modo de transmisión y el tipo de interacción que mantienen con sus hospedadores. 3) Finalmente, se ha estudiado el proceso de diversificación evolutiva a escala macro y icroevolutiva. La primera parte de la tesis presenta una base de datos global de relaciones ácaroave resultado de una extensa compilación de datos ya presentes en la literatura. También evalua y ajusta metodologías de “DNA barcoding” y “metabarcoding” para el estudio de los ácaros de las plumas. La segunda parte, revela a los ácaros de las plumas como simbiontes altamente especialistas en términos de hospedador cuyo modo de transmisión principal es el vertical. Por otro lado, el análisis de la dieta de los ácaros los sitúa como simbiontes comensales-mutualistas de las aves. Finalmente, la ultima parte de la tesis demuestra que la especiación por salto de hospedador es el proceso principal de diversificación de este grupo de simbiontes. Asimismo, también demuestra que los saltos de hospedador a larga distancia, a pesar de ser muy raros son muy relevantes para la diversificación de este grupo. Por último, los análisis de simbiontes encontrados en hospedadores inesperados (“stragglers”) revelan que este proceso es más prevalente de lo que se pensaba, y que sigue un patrón compatible con que está modulado por filtros ecológicos. A pesar de que los ácaros de las plumas se revelan como altamente especializados y específicos en términos de hospedador, su escenario coevolutivo es muy dinámico. El proceso de “straggling” y de cambio de hospedador son procesos prevalentes que permiten colonizar nuevos hospedadores. De acuerdo con esto, los procesos de coevolución y codiversificación en estos organismos no operan de manera aislada para cada pareja de hospedador y simbionte, si no de una manera similar a un mosaico geográfico de coevolución. Finalmente, el encaje ecológico y la competencia intraspecífica se identifican como los factores potencialmente más relevantes en las dinámicas (co)ecoevolutivas

Trees, Fungi, Insects: How Host Plant Genetics Builds a Community

Organisms, such as fungi and insects, can cause millions of acres of agricultural and forest damage, while others provide billions of dollars in ecological services such as education, aesthetic enjoyment, pollination, and gardening. Plant breeding and biotechnology can potentially help establish a balance between the proliferation of detrimental pests and attraction of beneficial insects. Variation in plant physiological and morphological characteristics are extremely important in the ability of host tissues to support many different types of organisms. When that variation is genetically heritable in a plant population, shifts in the underlying genes can have predictable consequences in structuring entire ecosystems. The field of community genetics seeks to study these interactions and identify the genes important in host plants, which will ultimately allow for the prediction of community level responses to changing conditions. The main goal of my dissertation was to identify the genetic underpinnings of host plant-biotic community organization in species belonging to the Salicaceae family, which contains many species of trees and shrubs of ecological and economic importance. To date, community genetic research has established the ability of hybrid plants to have wide-ranging heritable effects on communities and ecosystems. However, only a few publications have identified the genes underlying these relationships in pure species. In chapter 2, I utilized a pseudo-backcross hybrid family of Populus and quantitative trait analysis (QTL) as well as genomic comparisons of the P. trichocarpa and P. deltoides parents to identify potential candidate genes mediating their relationship with several insect herbivores and fungal pathogens. I found that many gene candidates had undergone recent tandem duplication and this pattern was enriched relative to the rest of the genome in the native parent QTL intervals. Additionally, I found the hybrids were mediating interactions between pathogens leading to unique genetic associations that would not normally be observed in a single species population, which may contribute to the elevated community effects that have been previously observed in natural hybrid zones. In chapter 3, I used surveys that were conducted in multiple common gardens of a population of P. trichocarpa, genome wide association analysis (GWAS), and networks to identify genes and potential biological functions underlying arthropod community composition. I found that genes associated with individual arthropods appeared to be very functionally targeted with rare variants related to metabolite production and manipulation of tissue nutrition. Genes that associated with arthropod richness and community composition have biological functions that may allow them to more broadly target multiple groups of arthropods, such as terpenoid synthesis, RNA inhibition, and transmembrane protein activity. In chapter 4, I used visual observation and pan-traps to survey the tree species Salix nigra and explore the impact of dioecy on the assembly of floral insect communities. I found that male trees supported higher diversity of floral visitors on their catkins when compared to females due to visual cues of yellow pollen. I also identified the main cross-pollinators to be three species of Andrena bees, one of which (A. nigrae) showed a preference for female flowers and was correlated to specific VOC cues from catkins. Finally, I detected an asynchrony in catkin bloom and insect emergence in early spring that threatens not only the sexual reproduction of S. nigra trees, but also the iii survival of local A. nigrae populations. Overall, I found that the dynamic plant-pathogen-herbivore-pollinator relationships are dependent on combinations of plant genetic effects with spatial and temporal environmental variability