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Decoupled Evolution of Floral Traits and Climatic Preferences in a Clade Of Serrano-Serrano et al. BMC Evolutionary Biology (2015) 15:247 DOI 10.1186/s12862-015-0527-6 RESEARCHARTICLE Open Access Decoupled evolution of floral traits and climatic preferences in a clade of Neotropical Gesneriaceae Martha Liliana Serrano-Serrano1,2, Mathieu Perret3, Maïté Guignard1, Alain Chautems3, Daniele Silvestro1,2,4 and Nicolas Salamin1,2* Abstract 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. Keywords: Brazilian Atlantic forest, Hummingbird pollination, Traitgram, Resupination, Pollination syndrome, Trait evolution, Comparative methods Background species [1]. Traits related to different niche axes are ex- Throughout the evolutionary process, lineages may ex- pected to follow different evolutionary trajectories that perience divergent modifications of their phenotype and may reflect different selection pressures, genetic con- genome that culminate with the establishment of separ- straints or stages of diversification determining the order ate species. Modeling the evolution of species traits can in which the different ecological axes are partitioned help to elucidate the likely sequence of diversification during species divergence [2]. For example, patterns of events that lead to phenotypically diverse groups of trait divergence during the diversification of live oaks (Ceanothus) in California suggested that traits related to * Correspondence: [email protected] local scale coexistence show an early divergence in the 1 Department of Ecology and Evolution, University of Lausanne, 1015 group, while traits related to large scale habitat display a Lausanne, Switzerland 2Swiss Institute of Bioinformatics, Quartier Sorge, 1015 Lausanne, Switzerland later or throughout differentiation [3]. Although Full list of author information is available at the end of the article © 2015 Serrano-Serrano et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Serrano-Serrano et al. BMC Evolutionary Biology (2015) 15:247 Page 2 of 12 theoretical work supports similar scenarios [1] empirical test if traits related to flower shape and size better fits a support for this model in other plant groups and across pollinator shift model involving transitions between different types of traits still needs to be evaluated. adaptive peaks defined by pollinator morphology and be- Hypotheses about the ordering of trait divergence havior [12], or if flowers have diversified regardless of during the evolution of a lineage can be complemen- the pollinator type. Second, we determine if the evolu- ted by investigating the mode and tempo of trait di- tion of climatic preferences is best explained by a model versification within lineages [4]. For instance, initially with distinct ecological optima [13] or a model with rapid morphological evolution followed by relative more labile evolution of climatic preferences among stasis [5] could be the result of new ecological oppor- closely related species [14]. To address these questions tunities accompanied by density-dependent slowdowns we first infer phylogenetic relationships among the spe- in species diversification [6, 7]. To explore this cies using multi-gene DNA sequences. We quantify the process, trait evolution can be reconstructed along floral morphology and climatic space occupied by the the branches of phylogenetic trees to detect hetero- group and, examine the tempo and mode of evolution of geneity in evolutionary rates through time, across lin- different traits in the CCN group using current models eages or in relation to discrete characters [8–10]. of trait evolution. We finally develop a new approach to Furthermore, Ornstein-Uhlenbeck (OU) models can visualize the estimated trait evolution by proposing an be used to describe bounded phenotypic evolution, alternative way to incorporate information from complex wheresingleormultipleselectiveregimespullpheno- models. Our results suggest that phenotypic evolution of types towards optimum values [11]. In plants, these this group is described by a variety of processes with dif- models have helped to understand the evolutionary ferent mode, time and lineage-specific effects. A new dynamics of flower morphology [12] and climatic visualization of complex models of trait evolution fur- niche [13]. Multiple studies have identified heteroge- ther allows a better understanding of the particular pro- neous rates of evolution across climate dimensions in cesses at play in this group of Neotropical plants. specific clades [14] and, at a larger scale, rates of niche evolution within major groups of angiosperms Methods that are dependent on the type of growth form [15]. Phylogenetic analyses The possibility of testing multiple models to reveal Taxonomic sampling included 46 out of the 52 species complex patterns of trait evolution during species di- in the group, as well as 13 outgroup species. Six molecu- versification is an important advantage to understand lar makers, two nuclear (ITS and ncpGS) and four plas- the dynamics of trait evolution and differential evolu- tid regions (atpB-rbcL spacer, rpl16 intron, rps16 intron, tion among traits [7, 16, 17]. However, the fit be- trnL-trnF spacer) were sequenced and aligned for a final tween the current models and the real evolutionary DNA matrix of 4.484 bp. We reconstructed phylogenetic processes is widely discussed [5, 18], and the power relationships and relative divergence times using for selecting models depends on the number of taxa, MrBayes and BEAST [28, 29]. Best fitting nucleotide the shape of the phylogeny, and the presence of mea- substitution models were estimated with the phymltest surements errors [19]. function in the R package ape [30]. Log-normal uncorre- In this study, we investigate the evolutionary history of lated relaxed clock and the Yule speciation priors were floral morphology and climatic preferences in a clade of set for the analyses. We used a maximum clade credibil- epiphytic plants belonging to the genera Codonanthop- ity (MCC) tree and a sample of high posterior probabil- sis, Codonanthe, and Nematanthus (hereafter referred to ity trees from the BEAST results for later analyses. as the CCN clade) of the Gesneriaceae family. This Finally, we examined the evolution of three binary traits group provides an excellent opportunity to compare (geographic distribution, pollination syndromes, and patterns of evolutionary diversification between these floral orientation) by reconstructing their ancestral states niche axes. CCN clade exhibits a remarkable floral diver- in the R package corHMM [31]. Detailed description of sity in shape, size and orientation reflecting potential the molecular dataset, phylogenetic reconstructions, and adaptation to different pollinators including bees and ancestral state estimation are provided in the Additional various hummingbirds [20–25]. Furthermore, CCN clade file 1: Appendix S1. is widely distributed throughout most Neotropical rainforest but present the highest species richness and Morphometric data level of range overlap in the Brazilian Atlantic Forest Thirteen quantitative
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