Edward G. LeBrun, Melissa Jones, Robert M. Plowes, and Lawrence E. Gilbert

PNAS March 28, 2022 | 119 (14) e2114558119

Significance

Invasive social insects are among the most damaging of invasive organisms and have proved universally intractable to biological control. Despite this, populations of some invasive social insects collapse from unknown causes. We report long-term studies demonstrating that infection by a microsporidian pathogen causes populations of a globally significant invasive ant to collapse to local extinction, providing a mechanistic understanding of a pervasive phenomenon in biological invasions: the collapse of established populations from endogenous factors. We apply this knowledge and successfully eliminate two large, introduced populations of these ants. More broadly, microsporidian pathogens should be evaluated for control of other supercolonial invasive social insects. Diagnosing the cause of unanticipated population collapse in invasive organisms can lead to applied solutions.

Abstract

Boom-bust population dynamics are a recurrent, widespread, and typically unexplained property of many species invasions. Declines also occur in invasive social insects from unknown causes. Nevertheless, social insects have proved intractable to biological control. Tawny crazy ants, an environmentally damaging invasive pest in several countries globally, are spreading in North America. Examining 15 local populations spanning 9 y, we document both the collapse of local populations of this ant in North America and a strong association of collapse with infection by the microsporidian pathogen, Myrmecomorba nylanderiae. Over the observation period, all longitudinally sampled local populations that harbored the pathogen declined, with 62% of these populations disappearing entirely. We test the causality of this relationship by introducing this pathogen into two local populations. At both sites, within 7 mo the pathogen was nearly universally prevalent, and within 2 y, tawny crazy ants were eliminated. In contrast, uninfected populations showed no tendency to decline over a similar period. Concurrent laboratory studies indicate that colony fragments died out because infected workers do not survive long enough to bridge the gap created by normal, winter cessation of immature ant production. Population-level collapse occurred because the pathogen spread faster than colony fragments declined, eliminating the density-dependent regulation seen with many pathogens. Invasive species beset by such pathogens may collapse if factors favoring transmission, like genetic homogeneity, high population density, or socially facilitated intragroup transmission, allow virulent pathogens to spread widely before disease impacts occur. These invasive species may be susceptible to boom-bust dynamics and pathogen-driven local extinction.

See https://www.pnas.org/doi/10.1073/pnas.2114558119