An Empirical Analysis Rejects the Hybrid Speciation Hypothesis of a Crucial Kiwifruit Species, Despite Genomic Evidence of Frequent Interspecific Gene Flow in the Genus.

Jie Yang,Ji Yang,Haoming Xu,Yuguo Wang,Weirui Fu,Wenju Zhang,Zhiping Song

doi:10.3389/fgene.2019.01250

Abstract

Hybrid speciation is an important way to generate species diversity. In general, however, interspecific hybridization is easily confused with the formation of hybrid species. Using the genomic resequencing data of the kiwifruit genus (Actinidia), at least ten species were documented recently as homoploid hybrid species, and thus a two-layer mode of species diversification has been proposed. As a crucial piece of evidence, Actinidia fulvicoma was identified as a hybrid derivative of Actinidia eriantha × Actinidia cylindrica, representing a rare case of hybrid species in kiwifruit that won the competition of ecological niches with one of its putative parental species, A. cylindrica. However, the hypothesized hybrid origin of A. fulvicoma is inconsistent with our specimen observations. Here, we present multiple lines of evidence to reject the hybrid speciation hypothesis for this species, despite genomic evidence for frequent interspecific gene flow. We collected the samples of A. fulvicoma in type locality and neighboring regions to contrast them with type specimen, and sequenced nuclear ribosomal DNA ITS, chloroplast trnL-trnF and mitochondrial nad2-i3, as well as four single-copy nuclear genes explored from kiwifruit genomes, to infer phylogenetic relationships among A. fulvicoma, its putative parental species, and their relatives. Our data definitely reveal that A. fulvicoma occupies an independent backbone lineage and it is not a hybrid. This study suggests that correct evolutionary applications on extensive surveys of the putative hybrid and its possible parents with strict criteria are necessary in the documentation of hybrid speciation to advance our understanding of the genomic basis of hybrid species.

Highlights

As one of the important evolutionary forces, natural hybridization occurs frequently in flowering plants
Our samples of A. fulvicoma from the type locality and adjacent areas were not similar to that of Liu et al (2017), which voucher picture showed that its morphology was like the two putative parental species, and specially, its fruit was nearly round, close to that of A. eriantha [See Figure S1 of Liu et al (2017)]
Our results did not support the result of Liu et al (2017), which suggested that A. cylindrica was the female parent of A. fulvicoma and A. eriantha the male parent

Summary

Introduction

As one of the important evolutionary forces, natural hybridization occurs frequently in flowering plants. The fact that most plant hybrid zones are limited to an extent implies that hybrids are on average less fit than their parents, at least in parental habitats (Coyne, 1996; Rieseberg, 1997). Two diploid species of Helianthus (H. annuus and H. petiolaris) produced three diploid species (H. anomalus, H. deserticola, and H. paradoxus) through ancient hybridization (Rieseberg et al, 1995; Gross and Rieseberg, 2005). These hybrids are distributed in deserts, salt-rich swamps, or other suitable open habitats that are not occupied by parent species, respectively. Despite the argument of whether these criteria are too stringent (Feliner et al, 2017; Schumer et al, 2018), there is no doubt that many putative hybrid species need to be re-tested

Methods

Results

Conclusion