Phylogeny and evolution of anomalous roots in Daviesia (Fabaceae : Mirbelieae)

The phylogeny of the Australian legume genus Daviesia was estimated using sequences of the internal transcribed spacers of nuclear ribosomal DNA. Partial congruence was found with previous analyses using morphology, including strong support for monophyly of the genus and for a sister group relationship between the clade D. pachyloma and the rest of the genus. A previously unplaced bird-pollinated species, anceps + D. D. epiphyllum, was well supported as sister to the only other bird-pollinated species in the genus, D. speciosa, indicating a single origin of bird pollination in their common ancestor. Other morphological groups within Daviesia were not supported and require reassessment. A strong and previously unreported sister clade of Daviesia consists of the two monotypic genera Erichsenia and Viminaria. These share phyllode-like leaves and indehiscent fruits. The evolutionary history of cord roots, which have anomalous secondary thickening, was explored using parsimony. Cord roots are limited to three separate clades but have a complex history involving a small number of gains (most likely 0-3) and losses (0-5). The anomalous structure of cord roots ( adventitious vascular strands embedded in a parenchymatous matrix) may facilitate nutrient storage, and the roots may be contractile. Both functions may be related to a postfire resprouting adaptation. Alternatively, cord roots may be an adaptation to the low-nutrient lateritic soils of Western Australia. However, tests for association between root type, soil type, and growth habit were equivocal, depending on whether the variables were treated as phylogenetically dependent (insignificant) or independent ( significant).

Trait decoupling promotes evolutionary diversification of the trophic and acoustic system of damselfishes.

Trait decoupling, wherein evolutionary release of constraints permits specialization of formerly integrated structures, represents a major conceptual framework for interpreting patterns of organismal diversity. However, few empirical tests of this hypothesis exist. A central prediction, that the tempo of morphological evolution and ecological diversification should increase following decoupling events, remains inadequately tested. In damselfishes (Pomacentridae), a ceratomandibular ligament links the hyoid bar and lower jaws, coupling two main morphofunctional units directly involved in both feeding and sound production. Here, we test the decoupling hypothesis by examining the evolutionary consequences of the loss of the ceratomandibular ligament in multiple damselfish lineages. As predicted, we find that rates of morphological evolution of trophic structures increased following the loss of the ligament. However, this increase in evolutionary rate is not associated with an increase in trophic breadth, but rather with morphofunctional specialization for the capture of zooplanktonic prey. Lineages lacking the ceratomandibular ligament also shows different acoustic signals (i.e. higher variation of pulse periods) from others, resulting in an increase of the acoustic diversity across the family. Our results support the idea that trait decoupling can increase morphological and behavioural diversity through increased specialization rather than the generation of novel ecotypes.

Decoupled evolution of floral traits and climatic preferences in a clade of Neotropical Gesneriaceae.

BACKGROUND: Major factors influencing the phenotypic diversity of a lineage can be recognized by characterizing the extent and mode of trait evolution between related species. Here, we compared the evolutionary dynamics of traits associated with floral morphology and climatic preferences in a clade composed of the genera Codonanthopsis, Codonanthe and Nematanthus (Gesneriaceae). To test the mode and specific components that lead to phenotypic diversity in this group, we performed a Bayesian phylogenetic analysis of combined nuclear and plastid DNA sequences and modeled the evolution of quantitative traits related to flower shape and size and to climatic preferences. We propose an alternative approach to display graphically the complex dynamics of trait evolution along a phylogenetic tree using a wide range of evolutionary scenarios. RESULTS: Our results demonstrated heterogeneous trait evolution. Floral shapes displaced into separate regimes selected by the different pollinator types (hummingbirds versus insects), while floral size underwent a clade-specific evolution. Rates of evolution were higher for the clade that is hummingbird pollinated and experienced flower resupination, compared with species pollinated by bees, suggesting a relevant role of plant-pollinator interactions in lowland rainforest. The evolution of temperature preferences is best explained by a model with distinct selective regimes between the Brazilian Atlantic Forest and the other biomes, whereas differentiation along the precipitation axis was characterized by higher rates, compared with temperature, and no regime or clade-specific patterns. CONCLUSIONS: Our study shows different selective regimes and clade-specific patterns in the evolution of morphological and climatic components during the diversification of Neotropical species. Our new graphical visualization tool allows the representation of trait trajectories under parameter-rich models, thus contributing to a better understanding of complex evolutionary dynamics.

Different rates of defense evolution and niche preferences in clonal and nonclonal milkweeds (Asclepias spp.).

Given the dual role of many plant traits to tolerate both herbivore attack and abiotic stress, the climatic niche of a species should be integrated into the study of plant defense strategies. Here we investigate the impact of plant reproductive strategy and components of species' climatic niche on the rate of chemical defense evolution in the milkweeds using a common garden experiment of 49 species. We found that across Asclepias species, clonal reproduction repeatedly evolved in lower temperature conditions, in species generally producing low concentrations of a toxic defense (cardenolides). Additionally, we found that rates of cardenolide evolution were lower for clonal than for nonclonal species. We thus conclude that because the clonal strategy is based on survival, long generation times, and is associated with tolerance of herbivory, it may be an alternative to toxicity in colder ecosystems. Taken together, these results indicate that the rate of chemical defense evolution is influenced by the intersection of life-history strategy and climatic niches into which plants radiate.

Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo

We describe a Bayesian method for investigating correlated evolution of discrete binary traits on phylogenetic trees. The method fits a continuous-time Markov model to a pair of traits, seeking the best fitting models that describe their joint evolution on a phylogeny. We employ the methodology of reversible-jump ( RJ) Markov chain Monte Carlo to search among the large number of possible models, some of which conform to independent evolution of the two traits, others to correlated evolution. The RJ Markov chain visits these models in proportion to their posterior probabilities, thereby directly estimating the support for the hypothesis of correlated evolution. In addition, the RJ Markov chain simultaneously estimates the posterior distributions of the rate parameters of the model of trait evolution. These posterior distributions can be used to test among alternative evolutionary scenarios to explain the observed data. All results are integrated over a sample of phylogenetic trees to account for phylogenetic uncertainty. We implement the method in a program called RJ Discrete and illustrate it by analyzing the question of whether mating system and advertisement of estrus by females have coevolved in the Old World monkeys and great apes.

Evolution and coevolution in mutualistic networks

A major current challenge in evolutionary biology is to understand how networks of interacting species shape the coevolutionary process. We combined a model for trait evolution with data for twenty plant-animal assemblages to explore coevolution in mutualistic networks. The results revealed three fundamental aspects of coevolution in species-rich mutualisms. First, coevolution shapes species traits throughout mutualistic networks by speeding up the overall rate of evolution. Second, coevolution results in higher trait complementarity in interacting partners and trait convergence in species in the same trophic level. Third, convergence is higher in the presence of super-generalists, which are species that interact with multiple groups of species. We predict that worldwide shifts in the occurrence of super-generalists will alter how coevolution shapes webs of interacting species. Introduced species such as honeybees will favour trait convergence in invaded communities, whereas the loss of large frugivores will lead to increased trait dissimilarity in tropical ecosystems.

Animal visual systems and the evolution of color patterns: Sensory processing illuminates signal evolution

Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receiver's visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.

When does female multiple mating evolve to adjust inbreeding? : Effects of inbreeding depression, direct costs, mating constraints, and polyandry as a threshold trait

Peer reviewed

When does female multiple mating evolve to adjust inbreeding? : Effects of inbreeding depression, direct costs, mating constraints, and polyandry as a threshold trait

Ackowledgements: This work was funded by a European Research Council Starting Grant to JMR. All simulations were performed using the Maxwell computing cluster at the University of Aberdeen

The Roles of Phenotypic Plasticity and Plant-Microbe Interactions in the Evolution of Complex Traits in Boechera stricta

All organisms live in complex habitats that shape the course of their evolution by altering the phenotype expressed by a given genotype (a phenomenon known as phenotypic plasticity) and simultaneously by determining the evolutionary fitness of that phenotype. In some cases, phenotypic evolution may alter the environment experienced by future generations. This dissertation describes how genetic and environmental variation act synergistically to affect the evolution of glucosinolate defensive chemistry and flowering time in Boechera stricta, a wild perennial herb. I focus particularly on plant-associated microbes as a part of the plant’s environment that may alter trait evolution and in turn be affected by the evolution of those traits. In the first chapter I measure glucosinolate production and reproductive fitness of over 1,500 plants grown in common gardens in four diverse natural habitats, to describe how patterns of plasticity and natural selection intersect and may influence glucosinolate evolution. I detected extensive genetic variation for glucosinolate plasticity and determined that plasticity may aid colonization of new habitats by moving phenotypes in the same direction as natural selection. In the second chapter I conduct a greenhouse experiment to test whether naturally-occurring soil microbial communities contributed to the differences in phenotype and selection that I observed in the field experiment. I found that soil microbes cause plasticity of flowering time but not glucosinolate production, and that they may contribute to natural selection on both traits; thus, non-pathogenic plant-associated microbes are an environmental feature that could shape plant evolution. In the third chapter, I combine a multi-year, multi-habitat field experiment with high-throughput amplicon sequencing to determine whether B. stricta-associated microbial communities are shaped by plant genetic variation. I found that plant genotype predicts the diversity and composition of leaf-dwelling bacterial communities, but not root-associated bacterial communities. Furthermore, patterns of host genetic control over associated bacteria were largely site-dependent, indicating an important role for genotype-by-environment interactions in microbiome assembly. Together, my results suggest that soil microbes influence the evolution of plant functional traits and, because they are sensitive to plant genetic variation, this trait evolution may alter the microbial neighborhood of future B. stricta generations. Complex patterns of plasticity, selection, and symbiosis in natural habitats may impact the evolution of glucosinolate profiles in Boechera stricta.

Molecular Systematics and Traits Evolution in Phasmatodea Leach, 1815 (Hexapoda; Insecta)

Phasmatodea Leach, 1815 (Hexapoda; Insecta) is a polyneopteran order which counts approximately 3000 described species, often known for their remarkable forms of mimicry. In this thesis, I provide a comprehensive systematic framework which includes over 180 species never considered in a phylogenetic framework: the latter can facilitate a better understanding of the processes underlying phasmids evolutionary history. The clade represents in fact an incredible testing ground to study trait evolution and its striking disparity of reproductive strategies and wing morphologies have been of great interest to the evolutionary biology community. Phasmids wings represent one of the first and most notable rejection of Dollo’s law and they played a central role in initiating a long- standing debate on the irreversibility of complex traits loss. Macroevolutionary analyses presented here confirm that wings evolution in phasmids is a reversible process even when possible biases - such as systematic uncertainty and trait-dependent diversification rates - are considered. These findings remark how complex traits can evolve in a dynamic, reversible manner and imply that their molecular groundplan can be preserved despite its phenotypical absence. This concept has been further tested with phylogenetic and transcriptomic approaches in two phasmids parthenogenetic lineages and a bisexual congeneric of the European Bacillus species complex. Leveraging a gene co-expression network approach, male gonad associated genes were retrieved in the bisexual species and then their modifications in the parthenogens were charachterized. Pleiotropy appears to constrain gene modifications associated to male reproductive structures after their loss in parthenogens, so that the lost trait molecular groundplan can be largely preserved in both transcription patterns and sequence evolution. Overall, the results presented in this thesis contribute to shape our understanding of the interplay between the phenotypic and molecular levels in trait evolution.

Understanding the concepts of community phylogenetics

Background: Community phylogenetics is an emerging field of research that has made important contributions to understanding community assembly. The rapid development of this field can be attributed to the merging of phylogenetics and community ecology research to provide improved clarity on the processes that govern community structure and composition. Question: What are the major challenges that impede the sound interpretation of the patterns and processes of phylogenetic community assembly? Methods: We use four scenarios to illustrate explicitly how the phylogenetic structure of communities can exist in stable or transient phases, based on the different combinations of phylogenetic relationships and phenotypic traits among co-occurring species. We discuss these phases by implicating a two-way process in the assembly and disintegration of the given ecological community. Conclusions: This paper synthesizes the major concepts of community phylogenetics using habitat filtering and competition processes to elucidate how the understanding of phylogenetic community structure is currently hindered by the dynamics of community assembly and disassembly.

Effects of phylogenetic signal on ancestral state reconstruction.

One of the standard tools used to understand the processes shaping trait evolution along the branches of a phylogenetic tree is the reconstruction of ancestral states (Pagel 1999). The purpose is to estimate the values of the trait of interest for every internal node of a phylogenetic tree based on the trait values of the extant species, a topology and, depending on the method used, branch lengths and a model of trait evolution (Ronquist 2004). This approach has been used in a variety of contexts such as biogeography (e.g., Nepokroeff et al. 2003, Blackburn 2008), ecological niche evolution (e.g., Smith and Beaulieu 2009, Evans et al. 2009) and metabolic pathway evolution (e.g., Gabaldón 2003, Christin et al. 2008). Investigations of the factors affecting the accuracy with which ancestral character states can be reconstructed have focused in particular on the choice of statistical framework (Ekman et al. 2008) and the selection of the best model of evolution (Cunningham et al. 1998, Mooers et al. 1999). However, other potential biases affecting these methods, such as the effect of tree shape (Mooers 2004), taxon sampling (Salisbury and Kim 2001) as well as reconstructing traits involved in species diversification (Goldberg and Igić 2008), have also received specific attention. Most of these studies conclude that ancestral character states reconstruction is still not perfect, and that further developments are necessary to improve its accuracy (e.g., Christin et al. 2010). Here, we examine how different estimations of branch lengths affect the accuracy of ancestral character state reconstruction. In particular, we tested the effect of using time-calibrated versus molecular branch lengths and provide guidelines to select the most appropriate branch lengths to reconstruct the ancestral state of a trait.

Measurement Errors Should Always Be Incorporated in Phylogenetic Comparative Analysis

The evolution of continuous traits is the central component of comparative analyses in phylogenetics, and the comparison of alternative models of trait evolution has greatly improved our understanding of the mechanisms driving phenotypic differentiation. Several factors influence the comparison of models, and we explore the effects of random errors in trait measurement on the accuracy of model selection. We simulate trait data under a Brownian motion model (BM) and introduce different magnitudes of random measurement error. We then evaluate the resulting statistical support for this model against two alternative models: Ornstein-Uhlenbeck (OU) and accelerating/decelerating rates (ACDC). Our analyses show that even small measurement errors (10%) consistently bias model selection towards erroneous rejection of BM in favour of more parameter-rich models (most frequently the OU model). Fortunately, methods that explicitly incorporate measurement errors in phylogenetic analyses considerably improve the accuracy of model selection. Our results call for caution in interpreting the results of model selection in comparative analyses, especially when complex models garner only modest additional support. Importantly, as measurement errors occur in most trait data sets, we suggest that estimation of measurement errors should always be performed during comparative analysis to reduce chances of misidentification of evolutionary processes.

Evidence for adaptive radiation from a phylogenetic study of plant defenses.

One signature of adaptive radiation is a high level of trait change early during the diversification process and a plateau toward the end of the radiation. Although the study of the tempo of evolution has historically been the domain of paleontologists, recently developed phylogenetic tools allow for the rigorous examination of trait evolution in a tremendous diversity of organisms. Enemy-driven adaptive radiation was a key prediction of Ehrlich and Raven's coevolutionary hypothesis [Ehrlich PR, Raven PH (1964) Evolution 18:586-608], yet has remained largely untested. Here we examine patterns of trait evolution in 51 North American milkweed species (Asclepias), using maximum likelihood methods. We study 7 traits of the milkweeds, ranging from seed size and foliar physiological traits to defense traits (cardenolides, latex, and trichomes) previously shown to impact herbivores, including the monarch butterfly. We compare the fit of simple random-walk models of trait evolution to models that incorporate stabilizing selection (Ornstein-Ulenbeck process), as well as time-varying rates of trait evolution. Early bursts of trait evolution were implicated for 2 traits, while stabilizing selection was implicated for several others. We further modeled the relationship between trait change and species diversification while allowing rates of trait evolution to vary during the radiation. Species-rich lineages underwent a proportionately greater decline in latex and cardenolides relative to species-poor lineages, and the rate of trait change was most rapid early in the radiation. An interpretation of this result is that reduced investment in defensive traits accelerated diversification, and disproportionately so, early in the adaptive radiation of milkweeds.