Evolution of antagonistic and mutualistic traits in the yucca‐yucca moth obligate pollination mutualism

Abstract

Species interactions shape the evolution of traits, life histories and the pattern of speciation. What is less clear is whether certain types of species interaction are more or less likely to lead to phenotypic divergence among species. We used the brood pollination mutualism between yuccas and yucca moths to test how mutualistic (pollination) and antagonistic (oviposition) traits differ in the propensity to increase phenotypic divergence among pollinator moths. We measured traits of the tentacular mouthparts, structures used by females to actively pollinate flowers, as well as ovipositor traits to examine differences in the rate of evolution of these two suites of traits among pollinator species. Morphological analyses revealed two distinct groups of moths based on ovipositor morphology, but no such groupings were identified for tentacle morphology, even for moths that pollinated distantly related yuccas. In addition, ovipositor traits evolved at significantly faster rates than tentacular traits. These results support theoretical work suggesting that antagonism is more likely than mutualism to lead to phenotypic divergence.

Components of local adaptation and divergence in pollination efficacy in a coevolving species interaction

“…Pollination by seed parasites has evolved repeatedly (e.g., Compton et al, 2010; Godsoe et al, 2008; Ibanez et al, 2009; Kawakita et al, 2019), and oviposition behavior ranges from laying eggs outside the ovary ( Silene ‐ Hadena : [Bopp & Gottsberger, 2004]; globeflower‐globeflower fly: [Pellmyr, 1989]) to laying eggs inside the ovary next to the ovules (yucca‐yucca moths: [Godsoe et al, 2008]; fig‐fig wasps: [Ghara et al, 2011]; Lithophragma ‐ Greya : [Thompson & Pellmyr, 1992]). On a less pronounced scale, oviposition behavior has been shown to also differ among species within a genus as in yucca moths (Althoff & Segraves, 2022) or within a species ovipositing on different hosts as in G. politella , which pierces the floral ovary through or just above the nectary disk in most Lithophragma species but slides its ovipositor through a slit between the elongated, unfused styles in L. bolanderi represented by plants from MBL (Thompson et al, 2013). We documented this differential oviposition behavior of G. politella even between L. bolanderi populations.…”

Trait matching in a multi‐species geographic mosaic of leafflower plants, brood pollinators, and cheaters

“…Trait matching between partners is usually expected to maintain mutualistic interactions, since in order for mutualisms to function, partner taxa must have traits which match, and thus such matching traits will be under strong stabilizing selection (Week & Nuismer, 2021; Yoder & Nuismer, 2010). In its most extreme forms, such as yuccas and yucca moths, and figs and fig wasps, insects and their host plants exhibit species‐specific reciprocal adaptation in both morphology and behaviors pertaining to pollination and oviposition (Althoff & Segraves, 2022; Kjellberg et al, 2001). At the same time, other mutualisms show coevolutionary arms race dynamics, in which trait mismatching is favored on one side of the interaction and trait matching is favored on the other (Anderson et al, 2010; Darwin, 1862; Nilsson, 1988).…”

“…At the same time, other mutualisms show coevolutionary arms race dynamics, in which trait mismatching is favored on one side of the interaction and trait matching is favored on the other (Anderson et al, 2010; Darwin, 1862; Nilsson, 1988). Brood pollination mutualisms may contain elements of both such dynamics because they contain both mutualistic (pollination) and antagonistic (seed predation) components (Althoff & Segraves, 2022). Despite the importance of trait matching and mismatching in mutualistic interactions, they have been primarily empirically demonstrated in specialized associations with few interacting species.…”

Coevolution-induced stabilizing and destabilizing selection shapes species richness in clade co-diversification

“…Under the trait-matching scenario (in the sense of Yoder and Nuismer 2010), on the other hand, a species’ coevolutionary fitness is maximized when its trait value more closely matches that of its interaction partner. Antagonistic examples of this scenario include brood parasitism (Langmore, Hunt, and Kilner 2003) whereas mutualistic examples including obligate pollination mutualisms (Althoff and Segraves 2022). Third, the strength of natural selection imposed by a species interaction is not always symmetrical for the interacting parties, with the selection often being much stronger on one party than on the other (Brodie and Brodie 1999; Andreazzi, Thompson, and Guimaraes Jr 2017; Endara et al 2017).…”