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

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.

Phylogeny, Age, and Evolution of Tribe Lilieae (Liliaceae) Based on Whole Plastid Genomes

“…Species of Lilieae dispersed in the temperate climatic regions of the northern hemisphere ( Boufford, 1993 ; Chen et al, 2000 ; Kiani et al, 2017 ): Cardiocrinum species spread over east Asia ( Ohara et al, 2006 ; Yang et al, 2016 ; Lu et al, 2020 ) and Notholirion species evolved as endemics in the Himalaya mountains ( Li et al, 2018 , 2020 ). Lilium and Fritillaria species are widely distributed in the northern hemisphere, and many Lilium species are densely distributed in east Asia ( Gao et al, 2013 ; Gao and Gao, 2016 , Gao et al, 2020 ; Givnish et al, 2016 ; Liu et al, 2018 ; Su et al, 2021 ), whereas species of Fritillaria are mainly distributed in central Asia and the Mediterranean region ( Wang et al, 2009 ; Day et al, 2014 ; Mustafa and Abdul-Razaq, 2015 ; Mucciarelli et al, 2016 ). Many species of Lilieae are distributed mainly in the southern and south-eastern regions of the QTP ( Wang et al, 2009 ; Gao et al, 2013 ; Li et al, 2020 ), consistent with the QTP being an intensive distribution center of Lilieae species ( Chen et al, 2000 ; Gao and Gao, 2016 ; Huang et al, 2018 ; Li et al, 2020 ).…”

When good species have porous boundaries: weak reproductive isolation and extensive gene flow between Mimulus glaucescens and M. guttatus in northern California

“…The notion that reproductively isolated or otherwise genetically distinct taxa could experience routine gene flow was historically controversial but has been widely reported more recently (Mebert 2008;Fitzpatrick et al 2008;Martin et al 2013;Harrison and Larson 2014;Gao et al 2020;Jiao and Yang 2020). Persistent gene flow despite significant reproductive barriers has been observed in diverse taxa (Fitzpatrick et al 2008;Larson et al the distinctive genetic coherence of M. glaucescens was supported based on the phylogenetic analysis (Fig.…”

“…The notion that reproductively isolated or otherwise genetically distinct taxa could experience routine gene flow was historically controversial but has been widely reported more recently (Mebert 2008; Fitzpatrick et al 2008; Martin et al 2013; Harrison and Larson 2014; Gao et al 2020; Jiao and Yang 2020). Persistent gene flow despite significant reproductive barriers has been observed in diverse taxa (Fitzpatrick et al 2008; Larson et al 2014; Richards et al 2018; Schield et al 2019), including other monkeyflowers (Brandvain et al 2014; Kenny and Sweigart 2016; Nelson et al 2021; Kiang and Hamrick 1978; Martin and Willis 2007; Case and Willis 2008; Fishman et al 2014; Kenny and Sweigart 2016; Schemske and Bradshaw 1999; Ramsey et al 2003).…”

Positive relationships among aboveground biomass, tree species diversity, and urban greening management in tropical coastal city of Haikou

“…We conducted the multiple regression analyses in two ways, with and without variable reduction to account for covariance. We reduced the number of variables using an approach that combines principle component analysis (PCA) with a UPGMA tree (Gao et al., 2020 ). First, we performed a PCA based on z‐transformations of all variables and generated a UPGMA tree using a Euclidean distance matrix to identify clusters of z ‐transformed variables.…”