Evolution of Plant Mating Systems

by

Alexander Harkness, Yaniv Brandvain, Emma Goldberg

• LAST REVIEWED: 11 January 2018
• LAST MODIFIED: 11 January 2018
• DOI: 10.1093/obo/9780199941728-0095

Introduction

Mating system has profound consequences for the ecology, distribution, and genetic structure of plant populations, and even the macroevolutionary fates of species and larger clades. “Mating system” is a notoriously ambiguous term, which we define operationally as the degree to which mating is random or nonrandom. This definition captures most of its common usage, at least as applied to plants. The most common form of nonrandom mating is inbreeding. When inbreeding is between separate but closely related individuals, it is called biparental inbreeding. Another form of inbreeding specific to hermaphroditic organisms is self-fertilization, also known as selfing. Although both forms are important, plant mating system research largely focuses on the rate of selfing. Inbred offspring are more homozygous than outcrossed offspring and thus exchange fewer alleles among their chromosomes when recombination occurs. Inbred populations have less allelic diversity than outcrossing populations, and the diversity they do have is sorted into homozygous lineages. Many plants have traits that reduce inbreeding, but why? Inbreeding depression—the decrease in offspring fitness caused by inbreeding—favors outcrossing. Selection to evade the expression of inbreeding depression by reducing inbreeding has in part shaped the remarkable diversity of floral architecture. Despite this, the evolutionary transition from outcrossing to self-fertilization is one of the most commonly traversed in flowering plants. What could overcome, repeatedly, the need for biparental sex that seems so common in eukaryotes? One of the most apparent theoretical advantages of self-fertilization over cross-fertilization is that a plant that can fertilize itself eliminates the liability of relying on pollinators or mates. This advantage might explain why selfing is more common in populations in which access to pollinators or conspecific mates is unreliable, such as frequently disturbed sites, edges of a species’ range, and locations reachable only by long-distance dispersal. A subtler advantage is that “selfers” may engage in a form of economic protectionism; pollen can fertilize self-ovules without needing to compete with pollen from other sires. Despite these advantages to an individual within a population, the reduction in genetic variation and effective recombination caused by selfing can limit future adaptation. Failure to adapt could lead to extinction. A species’ mating system, therefore, may be an essential determinant of its evolutionary lifespan.

General Overviews

The relative advantages of inbred and outbred mating systems in plants have been discussed since at least the 19th century. Barrett 2010 provides a detailed account of Darwin’s thoughts on mating system. In the 20th century, a series of canonical models for the evolution of self-fertilization arose from the field of population genetics. Charlesworth and Charlesworth 1979 clearly outlines the sequence of important models until the late 1970s, and Jarne and Charlesworth 1993 includes all current major models. Parallel to the development of theory, descriptive science has expanded the corpus of knowledge on the distribution of mating systems among taxa. Fryxell 1957 reviews mating system diversity in depth. Because both selfing and asexual reproduction require only a single parent, it is easy to conflate the two. Holsinger 2000 explains the key differences between selfing and asexual reproduction.

• Barrett, Spencer C. H. 2010. Darwin’s legacy: The forms, function and sexual diversity of flowers. Philosophical Transactions of the Royal Society of London B: Biological Sciences 365:351–368.

  DOI: 10.1098/rstb.2009.0212

  This high-level review evaluates adaptive explanations of the morphological diversity of flowers. It extensively catalogs different types of floral adaptations, including those that are less well known. The author traces modern discussion of the topic back to Darwin, who explained most floral adaptations as a means of maximizing outcrossing.

• Charlesworth, Deborah, and Brian Charlesworth. 1979. The evolutionary genetics of sexual systems in flowering plants. Proceedings of the Royal Society of London B: Biological Sciences 205:513–530.

  DOI: 10.1098/rspb.1979.0082

  The authors review the development of concepts in a chronological sequence of canonical models and relate how each built on previous work. This article provides the clearest view available of the historical context of models published previously.

• Fryxell, Paul A. 1957. Mode of reproduction of higher plants. The Botanical Review 23:135–233.

  DOI: 10.1007/BF02869758

  This taxonomically broad review classifies angiosperm mating systems based on frequency of cross-fertilization, self-fertilization, and asexual reproduction through seed (see Outcrossing Rate). It gives a sense of the proportions of species practicing these forms of reproduction.

• Holsinger, Kent E. 2000. Reproductive systems and evolution in vascular plants. Proceedings of the National Academy of Sciences 97:7037–7042.

  DOI: 10.1073/pnas.97.13.7037

  This review provides an introduction to the population genetic consequences of mating system in land plants. In particular, the comparison of the effects of self-fertilization and asexual reproduction reveals important symmetries while pointing out potential sources of confusion between them.

• Jarne, Philippe, and Deborah Charlesworth. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annual Review of Ecology and Systematics 24:441–466.

  DOI: 10.1146/annurev.es.24.110193.002301

  The authors of this review recommend a reorientation of mating system research toward an empirical focus. They argue that the possible theoretical advantages of selfing and outcrossing have been exhaustively described, but that basic data on selfing rate, inbreeding depression, and inbreeding coefficients are insufficient to decide their importance. The authors also explain the uses and limitations of some of the methods of estimating these parameters.