Antagonistic selection and pleiotropy constrain the evolution of plant chemical defenses

Abstract

When pleiotropy is present, genetic correlations may constrain the evolution of ecologically important traits. We used a quantitative genetics approach to investigate constraints on the evolution of secondary metabolites in a wild mustard, Boechera stricta. Much of the genetic variation in chemical composition of glucosinolates in B. stricta is controlled by a single locus, BCMA1/3. In a large‐scale common garden experiment under natural conditions, we quantified fitness and glucosinolate profile in two leaf types and in fruits. We estimated genetic variances and covariances (the G‐matrix) and selection on chemical profile in each tissue. Chemical composition of defenses was strongly genetically correlated between tissues. We found antagonistic selection between defense composition in leaves and fruits: compounds that were favored in leaves were disadvantageous in fruits. The positive genetic correlations and antagonistic selection led to strong constraints on the evolution of defenses in leaves and fruits. In a hypothetical population with no genetic variation at BCMA1/3, we found no evidence for genetic constraints, indicating that pleiotropy affecting chemical profile in multiple tissues drives constraints on the evolution of secondary metabolites.

Allelic differences of clustered terpene synthases contribute to correlated intra-specific variation of floral and herbivory-induced volatiles in a wild tobacco

“…The presence of genetic linkage and pleiotropy between HIPVs and floral volatiles suggest the evolution of plant volatiles might evolve under diffuse selection imposed from herbivores and pollinators in N. attenuata (Iwao & Rausher, 1997; Strauss & Irwin, 2004; Agrawal & Stinchcombe, 2009; Wise & Rausher, 2013). Diffuse coevolution can be common for plant resistance to multiple-herbivore communities (Wise & Rausher, 2013) and recent genetic analysis have discovered correlated changes of chemical defence compounds among tissues (Chan et al ., 2011; Keith & Mitchell-Olds, 2019) were due to genetic linkage or pleiotropy, similar to the two terpenoids we found here. Although future studies that use comparative metabolomics and transcriptomics are needed to further examine this, it is plausible that many other metabolic traits also show correlated changes among tissues.…”

“…Although future studies that use comparative metabolomics and transcriptomics are needed to further examine this, it is plausible that many other metabolic traits also show correlated changes among tissues. The diffuse interactions to multiple-herbivore communities and correlated changes of chemical defences among tissues often constrain the evolution of plant resistance (Wise & Rausher, 2013; Keith & Mitchell-Olds, 2019). Because plant-herbivore and plant-pollinator interactions were often studied in isolation (Lucas-Barbosa, 2016), to extent which diffused interaction exists among plant-herbivore and plant pollinator interactions, and what are the evolutionary consequences remain largely unclear.…”

Herbivore‐induced defenses are not under phylogenetic constraints in the genusQuercus(oak): Phylogenetic patterns of growth, defense, and storage

“…Trade‐offs may result from genetic associations between growth/reproduction and defense (antagonistic pleiotropy—reviewed in Hedrick, 1999; Johnson et al., 2015; Keith & Mitchell‐Olds, 2019; Rose, 1982; Wright, 1968) or from optimization strategies regarding nutrient acquisition and allocation (Metcalf, 2016; van Noordwijk & de Jong, 1986). Although antagonistic pleiotropy may be a plausible explanation for trade‐offs in Quercus species, an equally plausible hypothesis pertains to differences in nutrient acquisition and allocations to growth and defense (Bochdanovits & de Jong, 2004; van Noordwijk & de Jong, 1986; Ward & Young, 2002).…”

Evolutionary Genomics of Plant Gametophytic Selection

“…The evolutionary importance of the haploid gametophyte phase depends on what proportion of the genome is subject to selection. In addition, the impact of gametophytic selection on evolutionary processes can be constrained or accelerated by pleiotropic effects of gene function shared between the gametophytic and sporophytic stages ( Lande and Arnold 1983 ; Keith and Mitchell-Olds, 2019 ; and see below). Gene-expression studies, analyses of allelic variation in gametophytic success, and quantitative genetic analyses have all provided useful insights into the number of genes and fraction of mutations that are expressed in gametophytes, how their expression levels compare with sporophytic expression, and which mutations affect the success of both male and female gametophytes.…”