Phylogenomics, biogeography, and evolution of morphology and ecological niche of the eastern Asian–eastern North AmericanNyssa(Nyssaceae)

Abstract

Nyssa (Nyssaceae, Cornales) represents a classical example of the well‐known eastern Asian–eastern North American floristic disjunction. The genus consists of three species in eastern Asia, four species in eastern North America, and one species in Central America. Species of the genus are ecologically important trees in eastern North American and eastern Asian forests. The distribution of living species and a rich fossil record of the genus make it an excellent model for understanding the origin and evolution of the eastern Asian–eastern North American floristic disjunction. However, despite the small number of species, relationships within the genus have remained unclear and have not been elucidated using a molecular approach. Here, we integrate data from 48 nuclear genes, fossils, morphology, and ecological niche to resolve species relationships, elucidate its biogeographical history, and investigate the evolution of morphology and ecological niches, aiming at a better understanding of the well‐known EA–ENA floristic disjunction. Results showed that the Central American (CAM) Nyssa talamancana was sister to the remaining species, which were divided among three, rapidly diversified subclades. Estimated divergence times and biogeographical history suggested that Nyssa had an ancestral range in Eurasia and western North America in the late Paleocene. The rapid diversification occurred in the early Eocene, followed by multiple dispersals between and within the Erasian and North American continents. The genus experienced two major episodes of extinction in the early Oligocene and end of Neogene, respectively. The Central American N. talamancana represents a relic lineage of the boreotropical flora in the Paleocene/Eocene boundary that once diversified in western North America. The results supported the importance of both the North Atlantic land bridge and the Bering land bridge (BLB) for the Paleogene dispersals of Nyssa and the Neogene dispersals, respectively, as well as the role of Central America as refugia of the Paleogene flora. The total‐evidence‐based dated phylogeny suggested that the pattern of macroevolution of Nyssa coincided with paleoclimatic changes. We found a number of evolutionary changes in morphology (including wood anatomy and leaf traits) and ecological niches (precipitation and temperature) between the EA–ENA disjunct, supporting the ecological selection driving trait evolutions after geographic isolation. We also demonstrated challenges in phylogenomic studies of lineages with rapid diversification histories. The concatenation of gene data can lead to inference of strongly supported relationships incongruent with the species tree. However, conflicts in gene genealogies did not seem to impose a strong effect on divergence time dating in our case. Furthermore, we demonstrated that rapid diversification events may not be recovered in the divergence time dating analysis using BEAST if critical fossil constraints of the relevant nodes are not available. Our study provides an example of co...

Phylogenomics, biogeography, and evolution of the blue‐ or white‐fruited dogwoods (Cornus)—Insights into morphological and ecological niche divergence following intercontinental geographic isolation

“…Recent studies have shown pyRAD (Eaton, 2014) is a userfriendly and valuable pipeline for phylogenetic studies employing RAD-seq data (e.g., Qi et al, 2015;Zhou et al, 2018;Du et al, 2020;Zhou et al, 2020). pyRAD uses a VSEARCH (Rognes et al, 2016) method for clustering homologous sequences and allows for the inclusion of indel variation in the alignment.…”

“…The EA and ENA counterparts have been known to be highly similar morphologically (regarded as morphostasis), given their congeneric status, even though some of them may have been isolated since the Miocene (23.03-5.333 million years ago [Mya]; based on the GSA Geologic Time Scale v.5.0 used throughout) or earlier (Wen, 1999;Wen et al, 2010). However, this intuitive "morphostasis" of disjunct pairs has rarely been tested with careful morphological analysis (but see Du et al, 2020;Zhou et al, 2020). An explicit testing of the hypothesis would require a detailed comparison between the disjunct sisters and a comparison between each counterpart and the common ancestor of the disjunct clade.…”

“…An explicit testing of the hypothesis would require a detailed comparison between the disjunct sisters and a comparison between each counterpart and the common ancestor of the disjunct clade. Unfortunately, such studies have seldom been conducted (but see Du et al, 2020;Zhou et al, 2020). Estimating rates of morphological and molecular changes on branches of the phylogenetic tree will provide strong evidence for testing the hypothesis and shed light on how the rate of morphological evolution correlated with the rate of molecular evolution in the sister clades isolated in different geographic regions.…”

“…Estimating rates of morphological and molecular changes on branches of the phylogenetic tree will provide strong evidence for testing the hypothesis and shed light on how the rate of morphological evolution correlated with the rate of molecular evolution in the sister clades isolated in different geographic regions. Furthermore, comparison of abiotic environmental conditions between the disjunct counterparts can illuminate potential ecological drivers underlying the morphological changes (e.g., Du et al, 2020;Gaynor et al, 2020;Zhou et al, 2020). Therefore, studies characterizing and comparing morphological and abiotic environmental differences between disjunct pairs using a phylogenetic framework would be highly useful to address the questions of morphostasis and to better understand the evolution of EA-ENA disjunct floras post-isolation.…”

“…The DNA sequences, though likely represent a small portion of the genome, provide abundant genetic information across the genome for phylogenomic study. This approach has been shown to be useful in elucidating relationships of lineages across a wide range of divergence times, from the late Cretaceous to the late Neogene (e.g., Zhou et al, 2018Zhou et al, , 2020Du et al, 2020), though especially useful among closely related species (Eaton & Ree, 2013;Qi et al, 2015;Grewe et al, 2018;Zhou et al, 2018), with a relatively lower cost than most next-generation sequencing techniques (Baird et al, 2008;McKain et al, 2018).…”