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Replicated radiation of a plant clade along a cloud forest archipelago

Nature Ecology & Evolution volume 6, pages 1318–1329 (2022)Cite this article

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A Publisher Correction to this article was published on 04 August 2022

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Abstract

Replicated radiations, in which sets of similar forms evolve repeatedly within different regions, can provide powerful insights into parallel evolution and the assembly of functional diversity within communities. Several cases have been described in animals, but in plants we lack well-documented cases of replicated radiation that combine comprehensive phylogenetic and biogeographic analyses, the delimitation of geographic areas within which a set of ‘ecomorphs’ evolved independently and the identification of potential underlying mechanisms. Here we document the repeated evolution of a set of leaf ecomorphs in a group of neotropical plants. The Oreinotinus lineage within the angiosperm clade Viburnum spread from Mexico to Argentina through disjunct cloud forest environments. In 9 of 11 areas of endemism, species with similar sets of leaf forms evolved in parallel. We reject gene-flow-mediated evolution of similar leaves and show, instead, that species with disparate leaf forms differ in their climatic niches, supporting ecological adaptation as the driver of parallelism. Our identification of a case of replicated radiation in plants sets the stage for comparative analyses of such phenomena across the tree of life.

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Fig. 1: Phylogeny and biogeography of Oreinotinus.
Fig. 2: Leaf form evolution in Oreinotinus.
Fig. 3: Admixture and network analyses.
Fig. 4: Ecological differentiation of species with different leaf forms in Chiapas, Mexico.

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Data availability

All data are available in the Zenodo data repository https://doi.org/10.5281/zenodo.5504439.

Code availability

Scripts for reproducible science are in the GitHub repository at https://github.com/eaton-lab/Oreinotinus-phylogeny.

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Acknowledgements

Many colleagues have assisted us in the field, especially S. Madriñán (Colombia), D. Neill and J. Yepez (Ecuador), V. Torrez Flores and C. Maldonado (Bolivia), M. Isaura and M. Arakaki (Peru), K. Campbell (Jamaica), V. Alavez, J. Gómez, C. Martinez and S. Ramírez (Mexico). Herbaria in Colombia (ANDES, COL), Boliva (LPB), Ecuador (QCNE), Mexico (MEXU, ECOSUR) and Peru (USM) provided access to specimens and logistical support. For permission to work on their reserves (Cerro Huitepec and Moxviquil) we thank Pronatura Sur A.C. (C. Macías, S. Llamas, Ma. de los Ángeles Azuara and J. Gómez); the Asamblea de Bienes Comunales de Teopisca, Chiapas; I. Vázquez, H. Lara and D. Vázquez (Yashtinin, Chiapas); J. López (Huitepec, Oaxaca); and the Comisariados de Bienes Comunales of Santiago Comaltepec and Totontepec Villa de Morelos, Oaxaca. Our lab groups, T. Near and N. Mongiardino Koch provided useful comments. These studies were supported by NSF grants DEB-1557059 (M.J.D., D.A.R.E.), DEB-1753504 (E.J.E.) and DEB-2040347 (M.J.L.) and by the Botany Division of the Yale Peabody Museum of Natural History, the Departamento de Botánica, Instituto de Biología, UNAM and the Consejo Nacional de Ciencia y Tecnología, UNAM A1-S-26934 and IN210719 (M.E.O.).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA

    Michael J. Donoghue, Morgan K. Moeglein, Jordan R. Gardner, Nora M. Heaphy & Erika J. Edwards

  2. Peabody Museum of Natural History, Yale University, New Haven, CT, USA

    Michael J. Donoghue, Patrick W. Sweeney & Erika J. Edwards

  3. Department of Ecology, Evolution & Environmental Biology, Columbia University, New York, NY, USA

    Deren A. R. Eaton & Carlos A. Maya-Lastra

  4. Department of Biology, Washington University in St. Louis, St. Louis, MO, USA

    Michael J. Landis

  5. Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de Mexico, Mexico

    Mark E. Olson, N. Ivalú Cacho, Matiss Castorena & Alí Segovia Rivas

  6. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA

    Matiss Castorena

  7. Department of Biology, The College of New Jersey, Ewing, NJ, USA

    Wendy L. Clement

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  1. Michael J. Donoghue
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Contributions

Study design, funding, field studies, analyses and writing were carried out by M.J.D., D.A.R.E. and E.J.E. Additional contributions and analyses were performed by C.A.M.-L., M.J.L., P.W.S., J.R.G., N.M.H. and M.K.M. Field studies were also carried out by P.W.S., M.E.O., N.I.C., M.K.M., M.C., A.S.R. and W.L.C. Additional editing was carried out by C.A.M.-L., M.J.L., M.E.O. and N.M.H.

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Correspondence to Michael J. Donoghue, Deren A. R. Eaton or Erika J. Edwards.

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Nature Ecology & Evolution thanks Julia Day and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Individual-level RAD-seq tree for Oreinotinus.

ML tree inferred from concatenated RAD-seq data from 180 individuals of the Oreinotinus clade plus outgroups (see Methods). Specimen numbers are linked to voucher specimen information in Supplement Table 3. Bootstrap support values are shown at the nodes; black dots mark support of >85%. Accessions from multiple populations of the same morphology-based species form generally well-supported clades in all but five instances; these cases are discussed in the main text and in in Supplement Note 1.

Extended Data Fig. 2 Astral species tree for Oreinotinus.

Multispecies coalescent tree of 356 trees with more than 300 SNPs produced by ASTRAL-III (see Methods). Black nodes are supported by a local posterior probability > =85%.

Extended Data Fig. 3 Interactive species range map.

Points on the map represent all Oreinotinus localities included in our final vetted dataset, coloured by species and mapped using ArcGIS Pro (see Methods). Species are ordered by region in the legend, from north to south. Individual species ranges can be viewed by unchecking the boxes located in the left-hand panel to temporarily remove co-occurring species from the display. Clicking on a point will open a pop-up menu with metadata on the specimen attached to that point, including latitude and longitude, year of collection, institution and, where available, collector and specimen number. To view the distributions against a different background layer, such as topography or political boundaries, click ‘Basemap’ in the top bar.

Extended Data Fig. 4 Dimensionality reduction methods (UMAP and PCA) applied to SNP datasets with different filtering and imputation.

The subpanels included in Fig. 1 are outlined with black boxes (see Methods). (A) Our primary analyses filtered SNPs to require > =75% sample coverage at all SNPs and imputed the remaining data. Filtering with a higher minimum coverage thresholds (B-D) yielded highly similar results but began to lose statistical power when few SNPs were available at the highest thresholds. (E) An alternative K-means clustering method for assigning samples to groups for imputation recovered highly similar results as when using a priori population assignments. (E) UMAP projections show both local and global structure in the ‘All regions’ dataset, but do not reveal additional structure in the smaller datasets. These analyses also yielded similar results when imputed with Kmeans clustering (F).

Extended Data Fig. 5 Differentiation of leaf ecomorphs in Oreinotinus using nonmetric multidimensional scaling (NMDS).

A and C are based on three quantitative variables [leaf blade area, aspect ratio (leaf length/width) and the density of marginal teeth] and two categorical variables (a four-state character reflecting pubescence density and a two-state character for trichome type (see Methods). (A) Three clusters are identified by NMDS with K = 3; note that this lumps our IGE and SGE categories. (B) K = 3 is chosen as optimal by the inflection point in the inertia (sum of distances of samples to their closest cluster center); this represents a cutoff point where the inertia is not improved by adding extra Ks. (C) Within the IGE-SGE cluster, IGE and SGE species differ significantly in leaf blade area; these two ecomorphs are recognized on this basis for further phylogenetic and climatic comparisons. (D) Colours mark the four leaf ecomorphs recognized in this study (DEN, LPT, IGE, SGE) based on the totality of evidence; see main text and Fig. 2).

Extended Data Fig. 6 Ancestral reconstruction of leaf ecomorphs.

Ancestral states shown on the main tree represent 1,000 stochastic character mappings using ML transition matrix and the time-calibrated Oreinotinus phylogeny (Fig. 1). The smaller inset tree shows ancestral state reconstructions using parsimony on the same phylogeny. Our three quantitative characters are highlighted along the tips, with trait values standardized to a mean of zero and variance of 1. Bayesian stochastic mappings that account for phylogenetic uncertainty estimated a posterior median (and HPD95% interval) of 59 (28, 114) leaf form transitions (Supplement Note 3).

Extended Data Fig. 7 Additional ABBA-BABA tests focused on V. sulcatum.

Tests 1-8 show little discordance, suggesting that V. sulcatum has not been an introgressive donor into Eastern Mexican species of Viburnum. By contrast, tests 9-18 show much greater discordance when Eastern Mexican species are tested as introgressive donors into V. sulcatum compared to a taxon from Chiapas (V. jucundum) or Oaxaca (V. acutifolium). This suggests that V. sulcatum has introgressed with one or more species from the Eastern Mexican clade, but significance at the Z > 5 level is only seen in some tests and varies depending on the P3 and P1 taxa selected.

Extended Data Fig. 8 CHELSA climate variables generated from geo-referenced collection localities of V. hartwegii, V. jucundum and V. lautum on the Central Plateau of Chiapas, Mexico (see Methods).

We used the Wilcoxon rank sum test in R to compare the pairwise means of the three species. Box plot elements as follows: the center line corresponds to the median; the box limits represent upper and lower quartiles; and the whiskers span 1.5 x the interquartile range. Density ridgeline plots were drawn using the geom_density_ridges function from the ggridges R package96. N = 181 biologically independent samples (59 V. hartwegii, 65 V. jucundum, 57 V. lautum specimens).

Extended Data Fig. 9 Comparison of CHELSA climate variables that differ significantly in comparing V. hartwegii (IGE) to V. jucundum (LPT) and V. lautum (SGE) across the geographic range of Oreinotinus.

Compared across the entire range of Oreinotinus, IGE species differ significantly from LPT and SGE species in ways that align with our findings for the niches of the V. hartwegii in comparison with V. jucundum and V. lautum (see Methods). Specifically, we find that IGE species grow at lower elevations with higher temperatures and higher precipitation throughout the year, and lower temperature ranges and seasonality. Viburnum hartwegii was compared in detail with V. jucundum and V. lautum on the Central Plateau of Chiapas, Mexico (see Fig. 4). In making comparisons across the range of Oreinotinus we used data for the entire geographic ranges of our three focal species (that is, extending beyond the central Plateau of Chiapas; see Extended Data Fig. 3). Hypothesis testing method, box plot elements and density ridges formulation as in Extended Data Fig. 8. N = 2783 (1416 IGE, 713 LPT, 654 SGE specimens).

Extended Data Fig. 10 Comparison of CHELSA climate variables that differ significantly between V. jucundum (LPT) and V. lautum (SGE) across the geographic range of Oreinotinus.

Compared across the entire geographic range of Oreinotinus, LPT and SGE species differ significantly from one another in ways that align with our more detailed studies V. jucundum and V. lautum. Specifically, SGE species differ significantly from LPT species in their tendency to experience lower precipitation throughout the year, higher precipitation seasonality and higher seasonal and diurnal temperature ranges; SGE species may also tend to experience lower minimum temperatures in the coldest month. Viburnum jucundum and V. lautum were compared in detail on the Central Plateau of Chiapas, Mexico (see Fig. 4). In making comparisons across the range of Oreinotinus, we used data for the entire geographic ranges of these focal species (that is, extending beyond the central Plateau of Chiapas; see Extended Data Fig. 3. Hypothesis testing method, box plot elements and density ridges formulation as in Extended Data Fig. 8. N = 1367 (713 LPT and 654 IGE specimens).

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Supplementary Information

Supplementary Tables 1 and 2, Supplementary Figs. 1–15, Supplementary Notes 1–4 and Supplementary references.

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Supplementary Tables 3, 4 and 5

Supplementary Table 3. Specimens included in the individual-level Oreinotinus tree with collector information and RAD-seq information. Supplementary Table 4. ABBA-BABA statistics, taxon names and sample names for all admixture analyses. Supplementary Table 5. Oreinotinus leaf data.

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Donoghue, M.J., Eaton, D.A.R., Maya-Lastra, C.A. et al. Replicated radiation of a plant clade along a cloud forest archipelago. Nat Ecol Evol 6, 1318–1329 (2022). https://doi.org/10.1038/s41559-022-01823-x

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