Subtle, pervasive genetic correlation between the sexes in the evolution of dimorphic hummingbird tail ornaments*

Abstract

Male hummingbirds have repeatedly evolved sexually dimorphic tails that they use as ornaments during courtship. We examine how male ornament evolution is reflected in female morphology. Lande's two‐step model of the evolution of dimorphism predicts that γ (the genetic correlation between the sexes) causes trait elaboration to first evolve quickly in both sexes, then dimorphism evolves more slowly. On the hummingbird phylogeny, tail length does not fit this two‐step model; although hummingbirds repeatedly evolved ornamental, elongated tails, dimorphism evolves on the same phylogenetic branch as elongation, implying that γ quickly evolves to be low over phylogenetic timescales. Male “bee” hummingbirds have evolved diverse rectrix shapes that they use to produce sound. Female morphologies exhibit subtle, pervasive correlations with male morphology. No female‐adaptive hypotheses explain these correlations, since females do not also make sounds with their tail. Subtle shape similarity has arisen through the genetic correlation with males, and is subject to intralocus sexual conflict. Intralocus sexual conflict may produce increased phenotypic variation of female ornaments. Other evolutionary constraints on tail morphology include a developmental correlation between neighboring tail‐feathers, biasing tail elaboration to occur most often at the ends of the feather tract (rectrix 5 or 1) and not the middle.

Digest: Evolution of mutual ornamentation in hummingbirds*

“…This challenges the phylogenetic studies which showed higher frequency in gain and loss of ornaments in females compared to males (Wiens 2001) and which have been taken as evidence that female ornaments are genetically unconstrained. Though other studies have proposed genetic constraints or adaptive advantages as explanations for female ornamentation, Clark and Rankin (2020) show that genetic correlation could finely shape female ornament morphology across a bird family.…”

“…Clark and Rankin () do not find evidence for the sequence of events predicted by Lande in the phylogeny (Fig. ).…”

“…Male bee hummingbirds (tribe Mellisugini ) exhibit modifications in the shapes of their tail feathers, which are used during courtship dives to produce sounds for females. Clark and Rankin () observed subtle remains of these modifications in homologous female feathers. As females do not use their tail to produce sounds, the more parsimonious explanation is that female tail feathers have been retained as vestigial versions of male tail feathers, because of a genetic correlation between the sexes for the pattern of tail feather expression.…”

“…Phase I: sexual selection on males promotes the evolution of the ornamental trait in both sexes due to genetic correlation; Phase II: as the genetic correlation breaks down, sexes evolve under their own selective forces, and dimorphism occurs as a result of natural selection against expression of the character in females. (A) If the process is sufficiently slow, it might be possible to discern the different phases in the phylogeny, but (B) if the process is rapid, both trait exaggeration and sexual dimorphism could occur on the same branch, rendering the sequence of events invisible (as Clark and Rankin [] find in their study of the elongation of hummingbird tails).…”

“…In this issue, Clark and Rankin () use their knowledge of the Trochilidae family to investigate how male tail evolution is reflected in female morphology across this family. Male bee hummingbirds (tribe Mellisugini ) exhibit modifications in the shapes of their tail feathers, which are used during courtship dives to produce sounds for females.…”