Felsenstein’s “one-allele model” of speciation: The role of philopatry in the initial stages of host plant mediated reproductive isolation in Enchenopa binotata

Abstract

Abstract The study of speciation genetics is primarily concerned with identifying the genetic traits that allow divergent selection to overcome the homogenizing effects of gene flow. Felsenstein reviewed this race between gene flow and selection, concluding that speciation with gene flow was unlikely under a “two-allele model” (where two traits were necessary for reproductive isolation) but that divergence could occur quite easily under a “one-allele model.” Despite this finding, much of the sympatric speciation research involving phytophagous insects has relied on a two-trait model, where insects evolve both preferences for and increased performance on novel host plants. Philopatry (a tendency to remain where one was born) is known to occur in phytophagous insects and is a single trait isolation mechanism. However, it is traditionally invoked as simply augmenting reproductive isolation. Species in the Enchenopa binotata complex are believed to have speciated in sympatry. They exhibit host plant preferences, host specific performance advantages and strong philopatry. We experimentally shifted E. binotata to evolutionarily novel host plants. Previous research has demonstrated that the experimental population of insects possesses genetic variation in preference and performance to the novel host. The degree of philopatry at mating and egg-laying was assayed for the first four years under full choice conditions. Host plant preference and performance was assayed after eight years. Philopatry was an immediate and strong isolating mechanism, while preference for and performance on the novel host lagged. We therefore suggest that philopatry may be a more important mechanism in the early stages of a host shift than previously believed.