The phylogenetic history of the Gorteria diffusa radiation sheds light on the origins of plant sexual deception

Abstract

The morphologically diverse daisy species Gorteria diffusa employs varying levels of sexually deceptive pollination. The species comprises at least fifteen spatially and phenotypically discrete floral morphotypes that are associated with a range of pollination strategies, from generalism to highly specialised sexual deception involving visual mimicry of females of the bee-fly Megapalpus capensis. However, the pattern of evolution of the unique floral traits in this lineage remains unknown because the phylogenetic history of the closely related floral morphotypes has proved unresolvable using traditional approaches. Here we apply genotyping-by-sequencing (GBS), a reduced representation sequencing technology that has significantly increased the tractability of phylogenetic problems involving recent radiations, to the recalcitrant phylogenetic problem of Gorteria across its South African distribution. Population genomic analyses show that individuals group according to morphotype, irrespective of geographic proximity, highlighting the distinctiveness of the morphotypes at the genetic level. We resolve the phylogenetic history of the closely related morphotypes, demonstrating that they are mostly well supported monophyletic entities that are grouped into at least three distinct geographically separated clades. Our results suggest that both incomplete lineage sorting and introgression across geographical clades have previously hindered reconstruction of the phylogeny of this species complex that has diversified rapidly during the Quaternary. Sexual deception is a phylogenetically derived pollination strategy within the complex that evolved at least twice, and was likely achieved by sequential evolution of a set of floral traits that in combination elicit sexual responses from the bee-fly pollinator. While insight into the evolution of sexual deception has been limited by strong phylogenetic conservatism of this strategy in other plant lineages, our results both provide the framework, and confirm the utility of G. diffusa, for further understanding the genetic pathways and selective pressures underlying the complex phenotypes required to exploit insect mating behaviour for pollination.