Joint phylogenetic estimation of geographic movements and biome shifts during the global diversification ofViburnum

Abstract

<jats:title>Abstract</jats:title><jats:p>Phylogeny, fossils, biogeography, and biome occupancy provide evidence that reflects the singular evolutionary history of a clade. Despite the connections that bind them together, these lines of evidence are most often studied separately, by first inferring a fossil-dated molecular phylogeny, then mapping on ancestral ranges and biomes inferred from extant species. Here we jointly model the evolution of biogeographic ranges, biome affinities, and molecular sequences, incorporating fossils to estimate a dated phylogeny for all of the 163 extant species of the woody plant clade <jats:italic>Viburnum</jats:italic> (Adoxaceae) that we currently recognize. Our analyses indicate that while the major <jats:italic>Viburnum</jats:italic> lineages evolved in the Eocene, the majority of extant species originated since the Miocene. <jats:italic>Viburnum</jats:italic> radiated first in Asia, in warm, broad-leaved evergreen (lucidophyllous) forests. Within Asia we infer several early shifts into more tropical forests, and multiple shifts into forests that experience prolonged freezing. From Asia we infer two early movements into the New World. These two lineages probably first occupied warm temperate forests and adapted later to spreading cold climates. One of these lineages (<jats:italic>Porphyrotinus</jats:italic>) occupied cloud forests and moved south through the mountains of the Neotropics. Several other movements into North America took place more recently, facilitated by prior adaptations to freezing in the Old World. We also infer four disjunctions between Asia and Europe: the <jats:italic>Tinus</jats:italic> lineage is the oldest and probably occupied warm forests when it spread, while the other three were more recent and in cold-adapted lineages. These results variously contradict published accounts, especially the view that <jats:italic>Viburnum</jats:italic> radiated initially in cold forests and, accordingly, maintained vessel elements with scalariform perforations. We explored how the location and biome assignments of fossils affected our inference of ancestral areas and biome states. Our results are sensitive to, but not entirely dependent upon, the inclusion of fossil biome data. We argue that it will be critical to take advantage of all available lines of evidence to decipher events in the distant past, and the joint estimation approach developed here provides cautious hope even when fossil evidence is limited.</jats:p>

Fruit syndromes in Viburnum: correlated evolution of color, nutritional content, and morphology in bird-dispersed fleshy fruits

“…In previous phylogenetic reconstructions, V. clemensiae is placed as sister to the remainder of Viburnum. In Landis et al [22], the position of V. clemensiae is equivocal. It is either placed as sister to the rest of Viburnum or as sister to one of the two major subclades of Viburnum (containing Crenotinus + Valvatotinus + Pseudotinus + Urceolata).…”

“…For all Viburnum-wide trait evolution analyses, we used the phylogeny presented in Landis et al [22]. In brief, this phylogeny jointly estimates the phylogeny using a combination of molecular sequence data (restriction-site associated DNA sequencing [RAD-seq] data for 118 species, plus chloroplast and nuclear DNA for 153 species), biogeographic information, biome affinity, and morphological trait data.…”

“…To identify potential syndromes of fruit traits, we conducted a phylogenetic principal components analysis (PCA) using the R package phytools [46,47] in order to identify whether different fruit color categories (as perceived by humans) occupied different regions of PC space. To incorporate evolutionary relatedness, we used the phylogeny described above [22] and assumed a Brownian motion correlation structure for each trait. We chose five non-color fruit traits to include in the PC analyses that were likely to influence selection on fruit traits by dispersers: lipid content, moisture content, pulp volume, endocarp flatness (width/height ratio), and fruit width.…”

“…In this study, we use the flowering plant clade Viburnum as a model system to address these questions. Viburnum is a group of 163 species of mostly temperate forest shrubs and small trees of the Northern Hemisphere, although some species do occur in tropical regions of the Indo-Pacific as well as in cloud forests of Central and South America [22][23][24][25]. All Viburnum species produce fleshy, animal-dispersed drupe fruits and are largely birddispersed.…”

“…Viburnum fruits are borne in clusters (infructescences) of~20-100 fruits and display a wide variety of mature fruit colors, developmental patterns, and nutritional contents. Excellent knowledge of both the Viburnum phylogeny based on chloroplast and nuclear DNA sequences [22,26,27] and fruit traits of many species [24,26,28,29] make Viburnum ideal for a study of the evolution of fruit syndromes within putatively birddispersed species.…”