Abstract Detail

Symbioses: Plant, Animal, and Microbe Interactions

Hembry, David [1], Luo, Shi-Xiao [2], Liu, Tingting [2], Wang, Ziwei [2], Wu, Youheng [2], Duarte, Jesse [3], Fowler, Joshua [4], Whiteman, Noah [5], Dlugosch, Katrina [6].

When animal mutualists go bad: Repeated breakdown of a specialized pollination mutualism in leafflowers (Phyllanthaceae: Phyllanthus s. l.).

Although mutualism is commonly thought to be inherently unstable because of the opportunity for selection to favor antagonism by interacting partners, few macroevolutionary transitions from mutualistic symbiosis to parasitism have been reported. Leafflower moths (Lepidoptera: Gracillariidae: Epicephala) are distributed throughout tropical and warm temperate regions of the Old World, where most are specialized pollinating seed predators (in a manner analogous to fig wasps or yucca moths) of their host leafflower plants (Phyllanthaceae: Phyllanthus s. l.). Mutualistic leafflower moths actively pollinate their hosts’ flowers, but oviposit into the flowers’ ovaries, where the larvae consume a subset of the hosts’ seeds. This interaction is characterized by high biological intimacy, and thus has many parallels to fully symbiotic mutualisms. Multiple losses of pollination behavior—and therefore of mutualism—have been reported in the literature in leafflower moths in Asia. Here we report the discovery of non-pollinating leafflower moths associated with native species of leafflower plants (Phyllanthus spp.) in the southern United States (Oklahoma, Texas, Louisiana, and Florida). This is the first record of this high-intimacy plant-insect interaction from North America. Phylogenetic analysis of data from the literature combined with novel sequence data from Asia and North America reveals that this mutualism has broken down into parasitism at least seven times, and possibly more frequently. This mutualism has thus evolved into parasitism more frequently than any other mutualism known to date. We then use these repeated transitions and comparative framework to ask questions about the changes associated with mutualism breakdown in the biology of leafflower moths. We find that in some of these lineages, loss of mutualism is associated with transitions among distantly related host plants and colonization of new continents, suggesting that mutualism breakdown may in some cases offer substantial expansion of ecological opportunity. However, as far as is known, mutualism loss only occurs from the insect side of the interaction; no documented losses of moth pollination are known in Phyllanthus s. l. I discuss the implications of these findings for studies of mutualism loss in plant-animal interactions.

1 - Cornell University, Department of Entomology, Ithaca, NY, 14853, USA
2 - South China Botanical Garden, Guangzhou, Guangdong, China
3 - Pima Community College, Tucson, AZ, USA
4 - Rice University, Department of BioSciences, Houston, TX, USA
5 - University of California, Berkeley, Department of Integrative Biology, Berkeley, CA, 94720, USA
6 - University Of Arizona, ECOL AND EVOL BIOLOGY, P.O. Box 210088, Tucson, AZ, 85721, United States

Keywords:
mutualism
symbiosis
parasitism
Malpighiales
brood pollination
macroevolution.

Presentation Type: Oral Paper
Session: SYMB1, Symbioses: Plant, Animal, and Microbe Interactions
Location: Tucson J/Starr Pass
Date: Wednesday, July 31st, 2019
Time: 11:00 AM
Number: SYMB1012
Abstract ID:347
Candidate for Awards:None