Ting Zhang, K. Charlotte Jandér, Jian-Feng Huang, Bo Wang, Jiang-Bo Zhao, Bai-Ge Miao, Yan-Qiong Peng, and Edward Allen Herre

PNAS August 10, 2021 118 (32) e2021148118

Significance

Both the role of host sanctions (differential resource allocation to more beneficial symbionts) in stabilizing mutualisms, and the existence of “cheaters” (species gaining fitness by not benefiting their hosts) and their role in destabilizing them are controversial. A detailed study of an evolutionary transition from mutualism to parasitism focusing on two functionally distinct Eupristina wasp species associated with the fig, Ficus microcarpa in Yunnan Province, China, documents both. Within the comparative context of many existing studies of costs and benefits of active fig pollination, the results suggest that the low to nonexistent host sanctions on wasps that do not pollinate in this region promote the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.

Abstract

Theory identifies factors that can undermine the evolutionary stability of mutualisms. However, theory’s relevance to mutualism stability in nature is controversial. Detailed comparative studies of parasitic species that are embedded within otherwise mutualistic taxa (e.g., fig pollinator wasps) can identify factors that potentially promote or undermine mutualism stability. We describe results from behavioral, morphological, phylogenetic, and experimental studies of two functionally distinct, but closely related, Eupristina wasp species associated with the monoecious host fig, Ficus microcarpa, in Yunnan Province, China. One (Eupristina verticillata) is a competent pollinator exhibiting morphologies and behaviors consistent with observed seed production. The other (Eupristina sp.) lacks these traits, and dramatically reduces both female and male reproductive success of its host. Furthermore, observations and experiments indicate that individuals of this parasitic species exhibit greater relative fitness than the pollinators, in both indirect competition (individual wasps in separate fig inflorescences) and direct competition (wasps of both species within the same fig). Moreover, phylogenetic analyses suggest that these two Eupristina species are sister taxa. By the strictest definition, the nonpollinating species represents a “cheater” that has descended from a beneficial pollinating mutualist. In sharp contrast to all 15 existing studies of actively pollinated figs and their wasps, the local F. microcarpa exhibit no evidence for host sanctions that effectively reduce the relative fitness of wasps that do not pollinate. We suggest that the lack of sanctions in the local hosts promotes the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.

See https://www.pnas.org/content/118/32/e2021148118

Figure 1: Receptive F. microcarpa fig and pollinating structures of E. verticillata compared with Eupristina sp. (A) A cheater wasp (Eupristina sp.) laying eggs in a receptive fig of her host F. microcarpa. Pollinator wasps (E. verticillata) (B and C) have specialized morphological structures such as pollen pockets (black arrow) on the underside of their thorax and coxal combs on their forelegs (white arrows) that facilitate pollination. Pollen is stored in the pockets and coxal combs facilitate pollen transfer (43, 44). Cheater wasps (Eupristina sp.) (D and E) retain pollen pockets (black arrow) but lack coxal combs (white arrow).