A potential evolutionary trap for the extended phenotype of a nematomorph parasite

Human activities introduce new environmental cues to wild organisms, leading to maladaptive behavioral and life history decisions known as the “evolutionary trap.” This trap is thought to be a major conservation concern for free-living organisms. However, it has never been studied in endosymbionts, one of the most successful and diverse life forms on Earth. Here, we examine this trap in the extended phenotype of a parasite that exploits the visual system of hosts to alter host behavior for its benefit. Arboreal mantids infected by nematomorph parasites are drawn to horizontally polarized light, thereby inducing them to enter the water. In this study, we found that the degree of linear polarization (DOP) of reflected light served as a reliable environmental cue for identifying perennial waters, where nematomorphs can survive in their aquatic life stage without drying out. Infected mantids exhibit attraction to horizontally polarized light with higher DOP in behavioral assays and jumped into pools reflecting light with higher DOP in field experiments. The asphalt road reflected horizontally polarized light closely resembling the polarization levels observed in perennial waters, likely leading to a higher prevalence of mantids on asphalt roads compared with those found in natural arboreal habitats. In a field experiment, we observed infected mantids walking on asphalt roads more often than on cement roads. These findings imply that evolutionary traps can endanger endosymbionts beyond their hosts that directly perceive environmental cues.