The genetic architecture and evolution of life-history divergence among perennials in theMimulus guttatusspecies complex

Abstract

Ecological divergence is a fundamental source of phenotypic diversity between closely related species, yet the genetic architecture of most ecologically relevant traits is poorly understood. Differences in elevation can impose substantial divergent selection on both complex, correlated suites of traits (such as life-history), as well as novel adaptations. We use the Mimulus guttatus species complex to assess if the divergence in elevation is accompanied by trait divergence in a group of closely related perennials and determine the genetic architecture of this divergence. We find that divergence in elevation is associated with differences in life-history, as well as a unique trait, the production of rhizomes. The divergence between two perennials is largely explained by few mid-to-large effect quantitative trait loci (QTLs). However, the presence of QTLs with correlated, but opposing effects on multiple traits leads to some hybrids with transgressive trait combinations. Lastly, we find that the genetic architecture of the ability to produce rhizomes changes through development, wherein most hybrids produce rhizomes, but only later in development. Our results suggest that elevational differences may shape life-history divergence between perennials, but aspects of the genetic architecture of divergence may have implications for hybrid fitness in nature.

Indirect effects of parental conflict on conspecific offspring development

“…While a growing body of evidence has highlighted the role of parental conflict in the origins of reproductive isolation (namely HSI, and early-onset hybrid inviability in mammalian systems; (Vrana et al 1998, 2000; Brekke and Good 2014; Brekke et al 2016, 2021; Oneal et al 2016; Lafon-Placette et al 2018; Roth et al 2018 a ; Coughlan et al 2020 b ; Sandstedt et al 2020; Arévalo et al 2021)), the work presented here highlights a secondary role of parental conflict in speciation: hybridization between species that vary in their histories of parental conflict may result in indirect effects to intraspecific offspring development, in the event that intraspecific offspring develop alongside hybrids. In this system, M. guttatus co-occurs with both Northern and Southern M. decorus for large portions of their range (JMC personal obs; (Coughlan et al 2020 a )), and are thought to routinely hybridize and introgress (JMC unpublished data; (Puzey et al 2017)). Although seed size differences have been shown to influence several components of fitness in other systems (germination probability, seedling survivorship, flower production; (Stanton 1984; Simons and Johnston 2000; Gómez 2004)), these effects are likely to be context specific (for example, based on the competitive environment; (Stanton 1984)), and substantial fieldwork and further experimentation is required to quantify fitness effects in this system.…”

Taking quantitative genomics into the wild

“…Quantitative trait locus (QTL) mapping is an established approach that is still used to great effectiveness in well-phenotyped organisms where large numbers of molecular markers can be generated. Two studies in the issue used genotyping-by-sequencing data to identify QTLs; Lin et al [ 35 ] used an F 3 mapping population to map several fecundity QTLs in Boechera stricta (Drummond's rockcress), and Coughlan et al [ 36 ] used an F 2 mapping population from monkeyflowers Mimulus guttatus and M. decorus to identify 12 QTLs in six independent genomic regions associated with life-history traits important in local adaptation. The success of QTL mapping in controlled family crosses relies on generating co-inheritance of genetic markers and causal loci in subsequent generations.…”

One fish, two fish, red fish, dead fish: Detecting the genomic footprint of ecological incompatibilities

“…These mismatches may occur because which parent an F 1 resembles can differ between ecologically important traits (e.g., dominance mismatches [ 6 ]). Dominance mismatches are likely common between ecologically divergent species ([ 6 ]; examples include [ 7 , 8 ]). However, if the genetic architecture of ecological divergence is largely additive, trait mismatches may not manifest until recombination and independent assortment have reshuffled alleles to create individuals with alternate homozygous ancestry at 2 or more loci (akin to a fully recessive intrinsic incompatibility).…”