Prunus is a model clade for investigating tropical-to-temperate transitions

From Plant Press, Vol. 23, No. 2, April 2020.

By Richie Hodel

For over a century, biologists have observed a latitudinal gradient in species diversity in many clades across the Tree of Life, with greater species richness near the equator. However, we lack consensus about the cause of this biogeographic pattern and several hypotheses have been proposed. The tropical conservatism hypothesis (TCH) is one explanation for the observed latitudinal gradient; the TCH states that the relatively high biodiversity of the tropics is explained primarily by the geographic extent of tropical taxa during the past ~55 million years and the subsequent evolutionary conservation of environmental niches.

Recent large-scale phylogenetic studies using over 10,000 angiosperm species identified general trends describing how the latitudinal species gradient affects plant diversity. Notably, few lineages transitioned from tropical environments to temperate ones, which may be explained by the difficulty of acquiring the substantial adaptations necessary to tolerate the cooler conditions in temperate zones. One of the goals of my postdoctoral work at the National Museum of Natural History (NMNH) is to use the genus Prunus (Rosaceae) to test the TCH.

Prunus contains approximately 250-400 evergreen and deciduous species occurring throughout the temperate regions of the northern hemisphere and in the tropics and subtropics. Phylogenetic studies of Prunus have used several chloroplast and nuclear loci and produced key insights, but many questions remain. The phylogenetic position of Prunus within Rosaceae is uncertain, and phylogenetic relationships within Prunus are not yet fully resolved. Discord among chloroplast, nuclear, and morphological phylogenies suggests ancient polyploidy and/or hybridization may have impacted the evolutionary history of Prunus, and more data are needed to resolve the phylogeny (see figure below).

Cytonuclear discord in Prunus: the plastid phylogeny (left) infers a monophyletic racemose group, but the nuclear phylogeny (right) yields a paraphyletic racemose group. ‘A’ represents taxa in the Prunus-Amygdalus group, ‘B’ shows taxa in the Cerasus group, and ‘C’ depicts the polypoid racemose Prunus, which includes Laurocerasus, Padus, Pygeum, and Maddenia. The question mark shows the location on the phylogeny where ancient allopolyploidy may have occurred, leading to uncertain phylogenetic relationships in the racemose Prunus. Figure modified from Chin et al. 2014 and Zhao et al. 2016.

A phylogenomic analysis of Prunus using hundreds of nuclear loci is needed to resolve uncertain relationships, address the role of ancient hybridization and/or allopolyploidy in the evolution of Prunus, and serve as a framework for downstream analyses. One consequence of phylogenetic uncertainty is that the biogeographic history of Prunus remains uncertain, and subsequent analyses, such as tests of the TCH, are challenging. Because of its size, distribution, and an existing base of knowledge, Prunus will be an ideal clade for testing the TCH and investigating the processes that shape the latitudinal species gradient once phylogenetic relationships are resolved. Moreover, because of three documented tropical-to-temperate transitions in Prunus (solitary, corymbose, and racemose groups – see specimen images below), this genus represents a model system for investigating the dynamics and evolutionary implications of such transitions.

 

Herbarium sheets from the U.S. National Herbarium representing examples from (left to right) the solitary flower group of Prunus (P. persica; peach), the corymbose group of Prunus (P. avium; sweet cherry), and the racemose group of Prunus (P. serotina; blackcherry).

We are currently using targeted enrichment (Hyb-Seq) to generate hundreds of nuclear loci and entire chloroplast genomes for virtually all species in the genus. Jun Wen and collaborators have an extensive collection of tissue samples, which will be supplemented by field collections in southeast Asia, tentatively planned for early Fall 2020. Obtaining a complete-as-possible phylogeny of the genus is a critical first step. We will use the genomic data and the rich fossil record for this group to generate a time-calibrated phylogeny and infer diversification rates within Prunus. Geo-referenced distributional data will be combined with inferred diversification rates to investigate why tropical lineages diversify more rapidly than temperate clades.

We will also reconstruct the biogeographic history of Prunus, which will be possible with a fully resolved phylogeny with complete taxon sampling. Next, we can use the biogeographic results to define the patterns and processes of the tropical-temperate transitions. Ecological niche modeling analyses using geographic distribution data, phylogenomic data, and niche models derived from bioclimatic variables will be used to trace niche evolution in Prunus to test if differences in niche conservatism among lineages determine their current geographic distributions.

In some plants, key morphological characters are typically associated with tropical environments, such as entire leaf margins; in contrast, temperate species often have toothed or lobed leaf margins. Tropical and temperate members of Prunus have different leaf margin morphologies and may represent an opportunity to investigate how certain morphological characters facilitate tropical-to-temperate transitions. We will leverage digitized herbarium specimens from the U.S. National Herbarium for traditional morphological analyses and a machine learning approach developed by other researchers in the NMNH Botany Department to identify morphological characters important in key transitions in Prunus, including tropical-to-temperate transitions, diversification rate shifts, and niche evolution.

The COVID-19 pandemic has put some portions of this project into a holding pattern, such as lab work and collecting specimens in southeast Asia. I am currently working on a phylogeny to resolve the evolutionary history of cherries (subgenus Cerasus) using publicly available genomic resources. I am also working to assemble datasets of images from the U.S. National Herbarium to be used in machine learning analyses for identifying key characters associated with tropical-to-temperate transitions.