Exogenous selection rather than cytonuclear incompatibilities shapes asymmetrical fitness of reciprocal Arabidopsis hybrids.

Graham Muir,Polina Novikova,Roswitha Schmickl,Nora Hohmann,Paola Ruiz‐Duarte,Marcus A Koch,Barbara K Mable,Alessia Guggisberg

doi:10.1002/ece3.1474

Abstract

Reciprocal crosses between species often display an asymmetry in the fitness of F1 hybrids. This pattern, referred to as isolation asymmetry or Darwin's corollary to Haldane's rule, is a general feature of reproductive isolation in plants, yet factors determining its magnitude and direction remain unclear. We evaluated reciprocal species crosses between two naturally hybridizing diploid species of Arabidopsis to assess the degree of isolation asymmetry at different postmating life stages. We found that pollen from Arabidopsis arenosa will usually fertilize ovules from Arabidopsis lyrata; the reverse receptivity being less complete. Maternal A. lyrata parents set more F1 hybrid seed, but germinate at lower frequency, reversing the asymmetry. As predicted by theory, A. lyrata (the maternal parent with lower seed viability in crosses) exhibited accelerated chloroplast evolution, indicating that cytonuclear incompatibilities may play a role in reproductive isolation. However, this direction of asymmetrical reproductive isolation is not replicated in natural suture zones, where delayed hybrid breakdown of fertility at later developmental stages, or later-acting selection against A. arenosa maternal hybrids (unrelated to hybrid fertility, e.g., substrate adaptation) may be responsible for an excess of A. lyrata maternal hybrids. Exogenous selection rather than cytonuclear incompatibilities thus shapes the asymmetrical postmating isolation in nature.

Highlights

In many cases of hybridization, there is an asymmetry in the fitness of reciprocal F1 hybrid crosses (Tiffin et al 2001; Turelli and Moyle 2007; Bolnick et al 2008)
Significant asymmetries in the strength of reproductive isolation between A. arenosa and A. lyrata were found at both stages of isolation (Fig. 1A and B)
For crosses between A. lyrata 9 A. arenosa, seeds were produced in higher quantities than the reciprocal cross (Fig. 1A), with a twofold reduction when A. arenosa was the maternal parent

Summary

Introduction

In many cases of hybridization, there is an asymmetry in the fitness of reciprocal F1 hybrid crosses (Tiffin et al 2001; Turelli and Moyle 2007; Bolnick et al 2008). In Brassicaceae, SI is under the genetic control of a single locus, the S locus, which contains two tightly linked, highly polymorphic genes, S receptor kinase (SRK) expressed at the (female) stigmatic surface, and its ligand S locus cysteine-rich protein (SCR), expressed at the (male) pollen surface. These two recognition proteins determine the SI response (Schopfer et al 1999; Takasaki et al 2000; Takayama et al 2000; Silva et al 2001). Selfpollination is prevented when the SRK and SCR of an S allele express the same self-incompatibility type (reviewed in Ivanov et al 2010; Tantikanjana et al 2010; Iwano and Takayama 2012)

Methods

Results

Discussion

Conclusion