On the genetic architecture of rapidly adapting and convergent life history traits in guppies

The genetic basis of traits shapes and constrains how adaptation proceeds
in nature; rapid adaptation can be facilitated by polygenic traits, which
subsequently provide multiple, redundant, genetic routes to adaptive
phenotypes, reducing re-use of the same genes (genetic convergence). Guppy
life history traits evolve rapidly and convergently among natural high-
(HP) and low-predation (LP) environments in northern Trinidad. This system
has been studied extensively at the phenotypic level, but little is known
about the underlying genetic architecture. Here, we use an F2 QTL design
to examine the genetic basis of seven (five female, two male) guppy life
history phenotypes to assess whether the genetic architecture of these
traits reflects theoretical predictions. We use RAD-sequencing data
(16,539 SNPs) from 370 male and 267 female F2 individuals. We perform
linkage mapping, estimates of genome-wide and per-chromosome heritability
(multi-locus associations), and QTL ma pping (single-locus associations).
Our results are consistent with architectures of many-loci of small effect
for male age and size at maturity and female interbrood period. Male trait
associations are clustered on specific chromosomes, but female interbrood
period exhibits a weak genome-wide signal suggesting a potentially highly
polygenic component. Offspring weight and female size at maturity are also
associated with a single significant QTL each. These results suggest rapid
phenotypic evolution of guppies may be facilitated by polygenic trait
architectures, but these could fuel redundancy and limit gene re-use
across populations, in agreement with an absence of strong signatures of
genetic convergence from recent population genomic analyses of wild HP-LP
guppies.