Rapid experimental evolution of reproductive isolation from a single natural population

Significance

Darwin argued that differential natural selection across environments leads to the evolution of reproductive isolation and speciation. More recently, this process has been dubbed “ecological speciation.” Although simple in principle, mechanisms that link adaptation and reproductive isolation have seldom been demonstrated. We triggered diversification in the descendants of a single parasite population confined to different host “islands.” We used feather-feeding lice that pass their entire life cycle on the host, making it possible to evolve lice under natural conditions. Lineages of lice transferred to different sized pigeons rapidly evolved differences in size. These size differences reduced the ability of lice from different hosts to mate and reproduce. Our results effectively demonstrate how natural selection can cause species to form.

Abstract

Ecological speciation occurs when local adaptation generates reproductive isolation as a by-product of natural selection. Although ecological speciation is a fundamental source of diversification, the mechanistic link between natural selection and reproductive isolation remains poorly understood, especially in natural populations. Here, we show that experimental evolution of parasite body size over 4 y (approximately 60 generations) leads to reproductive isolation in natural populations of feather lice on birds. When lice are transferred to pigeons of different sizes, they rapidly evolve differences in body size that are correlated with host size. These differences in size trigger mechanical mating isolation between lice that are locally adapted to the different sized hosts. Size differences among lice also influence the outcome of competition between males for access to females. Thus, body size directly mediates reproductive isolation through its influence on both intersexual compatibility and intrasexual competition. Our results confirm that divergent natural selection acting on a single phenotypic trait can cause reproductive isolation to emerge from a single natural population in real time.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1901247116/-/DCSupplemental.