Why Self-fertilizing Plants Still Exist in Wild Populations: Diversity Assurance through Stress-Induced Male Sterility May Promote Selective Outcrossing and Recombination

Abstract

Climate change creates challenges for wild species, but plants have survived and adapted to similar changes in their evolutionary past. Most plants were originally outcrossing, one theoretical genetic reason being that self-fertilization does not create novel recombinants that allow adaptation. Thus selfing seems an evolutionary “dead end”. Nevertheless, self-fertilizing plants make up 14% of seed plant species. We offer a new interpretation of a response by self-fertilizing wild species to extreme existential threats, which creates novel recombinant progeny. This proposed mechanism goes beyond reproductive assurance, the usual explanation of selfing. Extreme stress, such as excessive heat within a specific window, first makes plants male-sterile, while female organs remain functional and can receive wind-borne pollen from any of the few nearby stress-tolerant individuals. Thus stress-induced male sterility enables and/or enhances outcrossing in selfing plants. Although in practice this proposed mechanism requires very special circumstances and operates only in certain species with conducive floral traits, we posit that over evolutionary time even such rare events can make a significant lasting impact on a species’ survival in changing conditions. This proposed mechanism, which we call Diversity Assurance, allows a population subject to severe stress to sample preferentially those genes that underpin tolerance to that specific stress. These genes are then recombined in subsequent generations, along with the male-sterility-under-stress trait of the female parent. This contributes in part to explain the effective evolution and hence persistence of self-fertilizing species. Diversity Assurance, we propose, is an adaptive mechanism that has been selected under extreme stress, underpinned by a simple loss-of-function of the male reproductive system. It may be triggered not only by heat, but also by other stressors. This proposed mechanism helps to explain why even highly self-fertilizing plant species remain able to respond to environmental changes through triggered outcrossing.

Introgression Breeding in Barley: Perspectives and Case Studies

“…Blended with existing seed stocks, the novel seeds would have led to the formation of heterogeneous mixtures of nearly homozygous lines (land races). Selection for novel phenotypes would increase their frequency in these land races, and the naturally occurring outcrossing (∼2%) that occurs in barley (Abdel-Ghani et al, 2004) and/or the environmentally induced outcrossing the can occur in selfing species (van Ginkel and Flipphi, 2020) would increase the frequency of favorable alleles introgressed into locally adapted genomes. Interestingly, many of the initial domestication traits remain critical in modern barley breeding.…”

Factors Influencing the Emergence of Heterogeneous Populations of Common Bean (Phaseolus vulgaris L.) and Their Potential for Intercropping

“…Flowers with functional female organs and non-functional male organs due to high temperature stress can be pollinated by foreign pollen when visited by bees or bumblebees, but only if the stigma is receptive to foreign pollen [ 61 , 64 ]. Altered growth conditions can lead to a greater diversity of offspring, which also increases the survival rate [ 65 ]. Another factor affecting outcrossing is the location of cultivation, which also depends on the type of pollinator; bumblebees are more attracted to bean flowers than bees [ 62 ].…”

Genomic Insights into High-Altitude Adaptation: A Comparative Analysis of Roscoea alpina and R. purpurea in the Himalayas

“…We speculated that different reproductive strategies and selection pressures may lead to differences in LD decay and population recombination rate. Self-fertilization is an adaptive strategy for plants in harsh environments, such as those where pollinators are absent [36,53,54]. Self-fertilization provides reproductive assurance under low levels of insect diversity in alpine ecosystems [55][56][57][58].…”