Hybrid Speciation and Introgression Both Underlie the Genetic Structures and Evolutionary Relationships of Three Morphologically Distinct Species of Lilium (Liliaceae) Forming a Hybrid Zone Along an Elevational Gradient.

Yundong Gao,Aj Harris,Huaicheng Li,Xinfen Gao

doi:10.3389/fpls.2020.576407

Abstract

We studied hybrid interactions of Lilium meleagrinum, Lilium gongshanense, and Lilium saluenense using an integrative approach combining population genetics, fieldwork, and phenological research. These three species occur along an elevational gradient, with L. meleagrinum occurring at lower elevations, L. saluenense at higher elevations, and L. gongshanense between them. The species show strong morphological differentiation despite there being no clear environmental barriers to gene flow among them. Lilium gongshanense is likely to have a hybrid origin based on our prior work, but its progenitors remain uncertain. We sought to determine whether gene flow occurs among these three parapatric species, and, if so, whether L. gongshanense is a hybrid of L. meleagrinum and/or L. saluenense. We analyzed data from multiple chloroplast genes and spacers, nuclear internal transcribed spacer (ITS), and 18 nuclear Expressed Sequence Tag-Simple Sequence Repeat (EST-SSR) microsatellites for accessions of the three species representing dense population-level sampling. We also inferred phenology by examining species in the field and using herbarium specimens. We found that there are only two types of chloroplast genomes shared among the three species and that L. gongshanense forms two distinct groups with closest links to other species of Lilium based on ITS. Taken together, L. gongshanense is unlikely to be a hybrid species resulting from a cross between L. meleagrinum and L. saluenense, but gene flow is occurring among the three species. The gene flow is likely to be rare according to evidence from all molecular datasets, and this is corroborated by detection of only one putative hybrid individual in the field and asynchronous phenology. We suspect that the rarity of hybridization events among the species facilitates their continued genetic separation.

Highlights

Natural hybridization, which may lead to hybrid speciation and/or genomic reticulation, is widely understood to be a major evolutionary mechanism in plants that can drive morphological change and adaptation, as well as shape biogeographic patterns (Soltis and Soltis, 2009)
We investigated the phylogenetic relationships among populations represented by haplotypes using the statistical parsimony procedure for phylogenetic network estimations implemented in TCS 1.21 (Clement et al, 2000) with a 95% criterion for parsimonious connections
We suspect that the LSn individual represents a rare hybrid of LS and LG because of its morphology, which is LSlike, and its genetic composition according to STRUCTURE (Figure 3 and Supplementary Figure 5) and the principal coordinates analyses (PCoA)

Summary

Introduction

Natural hybridization, which may lead to hybrid speciation and/or genomic reticulation, is widely understood to be a major evolutionary mechanism in plants that can drive morphological change and adaptation, as well as shape biogeographic patterns (Soltis and Soltis, 2009). Methods that explicitly test rates of introgression or complex evolutionary hypotheses (e.g., Anderson and Thompson, 2002; Beerli and Palczewski, 2010; Cornuet et al, 2014) are increasingly available and help to disentangle the complicated evolutionary histories of hybridizing taxa. These methods are complemented by careful examinations of morphology (e.g., to detect the prevalence of intermediate forms) and use of ecological indicators (e.g., to determine the degree to which parental species and hybrid offspring are environmentally compatible or incompatible). Case studies, such as in ragworts (Brennan et al, 2019; Nevado et al, 2020), azaleas (Yan et al, 2019), chestnuts (Sun et al, 2020), butterflies (Capblancq et al, 2019), birds (Hooper et al, 2019), and turtles (Scott et al, 2019), continue to provide valuable insights into the complex roles of hybridization and gene flow in evolution and speciation

Methods

Results

Discussion

Conclusion