The distribution of self-incompatibility systems in angiosperms: the relationship between mating system diversity, life span, growth habit and latitude in a changing global environment

Abstract

Background and aims: There is ample theoretical and experimental evidence that angiosperms harbouring self-incompatibility (SI) systems are likely to respond to global changes in unique ways relative to taxa with other mating systems. In this paper, we present an updated database on the prevalence of SI systems across angiosperms and examine the relationship between the presence of SI and latitude, biomes, life-history traits and management conditions to evaluate the potential vulnerability of SI taxa to climate change and habitat disturbance.

Methods: We performed literature searches to identify studies that employed controlled crosses, microscopic analyses and/or genetic data to classify taxa as having SI, self-compatibility (SC), partial self-compatibility (PSC) or self-sterility (SS). Where described, the site of the SI reaction and the presence of dimorphic versus monomorphic flowers were also recorded. We then combined this database on the distribution of mating systems with information about the life span, growth habit, management conditions and geographic distribution of taxa. Information about the geographic distribution of taxa was obtained from a manually curated version of the Global Biodiversity Information Facility database, and from vegetation surveys encompassing 9 biomes. We employed multinomial logit regression to assess the relationship between mating system and life-history traits, management condition, latitude and latitude-squared using self-compatible taxa as the baseline. Additionally, we employed LOESS regression to examine the relationship between the probability of SI and latitude. Finally, by summarizing information at the family level, we plotted the distribution of SI systems across angiosperms including information about the presence of SI or dioecy, the inferred reaction site of the SI system when known, as well as the proportion of taxa in a family for which information is available.

Key results: We obtained information about the SI status of 5686 hermaphroditic taxa, of which 55% exhibited SC, and the remaining 45% harbour SI, self-sterility (SS), or PSC. Highlights of the multinomial logit regression include that taxa with PSC have a greater odds of being short- (OR=1.3) or long- (OR=1.57) lived perennials relative to SC ones, and that SS/SI taxa (pooled) are less likely to be annuals (OR=0.64) and more likely to be long-lived perennials (OR=1.32). SS/SI taxa had a greater odds of being succulent (OR=2.4) or a tree (OR=2.05), and were less likely to be weeds (OR=0.34). Further, we find a quadratic relationship between the probability of being SI with latitude: SI taxa were more common in the tropics, a finding that was further supported by the vegetation surveys which showed fewer species with SS/SI in temperate and northern latitudes compared to mediterranean and tropical biomes.

Conclusions: We conclude that in the short-term habitat fragmentation, pollinator loss and temperature increases may negatively impact plants with SI systems, particularly long-lived perennial and woody species dominant in tropical forests. In the longer term, these and other global changes are likely to select for self-compatible or partially self-compatible taxa which, due to the apparent importance of SI as a driver of plant diversification across the angiosperm tree of life, may globally influence plant species richness.

Keywords: biome; database; geography; growth habit; latitude; life span; management; phylogeny; self-incompatibility; self-sterility.