Genetic potential for changes in breeding systems: Predicted and observed trait changes during artificial selection for male and female allocation in a gynodioecious species

Abstract

Premise Evolution of separate sexes from hermaphroditism often proceeds through gynodioecy, but genetic constraints on this process are poorly understood. Genetic (co‐)variances and between‐sex genetic correlations were used to predict evolutionary responses of multiple reproductive traits in a sexually dimorphic gynodioecious species, and predictions were compared with observed responses to artificial selection. Methods Schiedea (Caryophyllaceae) is an endemic Hawaiian lineage with hermaphroditic, gynodioecious, subdioecious, and dioecious species. We measured genetic parameters of Schiedea salicaria and used them to predict evolutionary responses of 18 traits in hermaphrodites and females in response to artificial selection for increased male (stamen) biomass in hermaphrodites or increased female (carpel, capsule) biomass in females. Observed responses over two generations were compared with predictions in replicate lines of treatments and controls. Results In only two generations, both stamen biomass in hermaphrodites and female biomass in females responded markedly to direct selection, supporting a key assumption of models for evolution of dioecy. Other biomass traits, pollen and ovule numbers, and inflorescence characters important in wind pollination evolved indirectly in response to selection on sex allocation. Responses generally followed predictions from multivariate selection models, with some responses unexpectedly large due to increased genetic correlations as selection proceeded. Conclusions Results illustrate the power of artificial selection and utility of multivariate selection models incorporating sex differences. They further indicate that pollen and ovule numbers and inflorescence architecture could evolve in response to selection on biomass allocation to male versus female function, producing complex changes in plant phenotype as separate sexes evolve.

A model for the gradual evolution of dioecy and heterogametic sex determination

“…While there is ample evidence for such variation in hermaphrodites across multiple taxa (recently shown in e.g. Mercurialis annua , Cossard et al, 2021, or Schiedea salicaria , Campbell et al, 2022; for reviews see Meagher, 1999, Table 1 in Ashman, 2003 and in Mazer et al, 2007), the specific loci responsible for this variation are not yet known for any species. In dioecious plants, the genetic basis of sex determination has been described in only a handful of species, with sex-determining loci consisting of either one master switch (e.g.…”

“…There is ample evidence for polygenic variation for sex allocation in many hermaphroditic taxa (as recently shown in e.g. Mercurialis annua , Cossard et al, 2021, or Schiedea salicaria , Campbell et al, 2022; for reviews see Meagher, 1999, Table 1 in Ashman, 2003 and in Mazer et al, 2007), but the specific loci involved are not yet known for any species. In dioecious plants, meanwhile, the specific genes involved in sex determination have only been described in a handful of species, with sex-determining loci consisting of either one master switch (e.g., in persimmon, poplar and willow, Akagi et al, 2014; Müller et al, 2020) or two fully-linked genes at which sterility mutations segregate as expected under the ‘two-gene model’ (e.g., in asparagus and kiwifruit, Akagi et al, 2019; Harkess et al, 2020; see also Westergaard, 1958 for phenotypic evidence consistent with this type of architecture).…”

What determines the evolutionary trajectories of wild plant species? Approaches to the study of quantitative fitness‐related traits

“…The evolution of separate sexes from hermaphroditism via an intermediate step of gynodioecy is common, but the genetic constraints influencing the transition are not well understood. Campbell et al (2022b) investigated models for the evolution of dioecy from hermaphroditism in Schiedea (Caryophyllaceae), an endemic Hawaiian genus with species expressing wide variation in reproductive systems. They assessed genetic variances and covariances of floral traits and inflorescence traits in the gynodioecious S. salicaria , a species presumably under selection for increased representation of females based on measures of self‐fertilization and inbreeding depression.…”