Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity

Abstract

SummaryOaks (Quercus, Fagaceae) are the dominant tree genus of North America in species number and biomass, and Mexico is a global center of oak diversity. Understanding the origins of oak diversity is key to understanding biodiversity of northern temperate forests.A phylogenetic study of biogeography, niche evolution and diversification patterns in Quercus was performed using 300 samples, 146 species. Next-generation sequencing data were generated using the restriction-site associated DNA (RAD-seq) method. A timecalibrated maximum likelihood phylogeny was inferred and analyzed with bioclimatic, soils, and leaf habit data to reconstruct the biogeographic and evolutionary history of the American oaks.Our highly resolved phylogeny demonstrates sympatric parallel diversification in climatic niche, leaf habit, and diversification rates. The two major American oak clades arose in what is now the boreal zone and radiated, in parallel, from eastern North America into Mexico and Central America.Oaks adapted rapidly to niche transitions. The Mexican oaks are particularly numerous, not because Mexico is a center of origin, but because of high rates of lineage diversification associated with high rates of evolution along moisture gradients and between the evergreen and deciduous leaf habits. Sympatric parallel diversification in the oaks has shaped the diversity of North American forests.

A nuclear DNA barcode for eastern North American oaks and application to a study of hybridization in an Arboretum setting

“…The sample set consisted of 228 acorns, 37 adult trees not previously genotyped (including nine mother trees), and 59 learning samples drawn from the 63 samples originally sequenced using RAD‐seq and used to identify SNPs. Maximum‐likelihood analysis of the SNP dataset from parent trees and learning samples recovers a topology comparable to that described in previous studies (Hipp et al., 2014, 2018; McVay, Hipp et al., 2017) (Figure 4). UPGMA analyses provide no additional insights over maximum‐likelihood analyses and are excluded from further discussion.…”

“…RAD‐seq DNA extraction, library preparation, and sequencing were conducted as presented previously in oaks (Cavender‐Bares et al., 2015; Hipp et al., 2014, 2018; McVay, Hauser et al., 2017, McVay, Hipp et al., 2017). Briefly, DNA for all RAD‐seq samples was extracted from fresh or frozen material using the DNeasy plant extraction protocol (DNeasy, Qiagen, Valencia, CA, USA).…”

“…The matrix of 119 SNPs was chosen for design of two final multiplexes to ensure a selection of 80 SNPs via the primer design suite across two multiplexes. Maximum‐likelihood (ML) phylogenetic analysis was then conducted for each matrix to evaluate whether each SNP set could identify species known from prior work (Hipp et al., 2018; McVay, Hipp et al., 2017) to be monophyletic. Phylogenetic analysis was conducted using PhyML (Guindon et al., 2010) with mode = “A la carte” and number of bootstraps = 100, as implemented in phylogeny.fr (Dereeper et al., 2008).…”

Host plant associations and geography interact to shape diversification in a specialist insect herbivore

“…Despite the growing assertion that macroevolutionary patterns of insect diversity do not necessarily follow an “escape and radiation” model (Hardy & Otto, ), there is long‐standing evidence that specialized insects can be used to infer the evolutionary history of their host (Ehrlich & Raven, ; Hafner & Nadler, ; Mitter, Farrell, & Futuyma, ), and there is precedent for classifying host plants and admixed lineages based on the distribution and performance of their insect herbivores (Abrahamson, Melika, Scrafford, & Csóka, ; Aguilar & Boecklen, ). Therefore, given the biogeographic history of live oaks, which includes geographically structured admixture among the host species used by B. treatae (Cavender‐Bares et al, ; Eaton et al, ; McVay et al, ), it is possible we underestimated the effect of HAD as a predictor of genomic variation in B. treatae in the dbRDA by limiting our analysis to the three nominal host plant taxa currently recognized (Hipp et al, ). Given the support for multiple B. treatae lineages within alternative host plants, it may be more appropriate to view contemporary populations of B. treatae as being distributed across live oak lineages that correspond to the entropy derived clusters of B. treatae more so than to the nominal plant taxa.…”

“…Belonocnema treatae is known from Qf in that part of the host plant's range extending into Mexico, and we have recently verified Q. oleoides in central Mexico as a host (Egan, personal observation). However, whether Q. brandegeei in Baja California, Q. sagraeana in Cuba or Q. oleoides into Central America (which is markedly differentiated from more northerly distributed Q. oleoides) (Cavender‐Bares et al, ; Hipp et al, ) are hosts of B. treatae is currently unknown.…”