Herbivore-mediated negative frequency-dependent selection underlies a trichome dimorphism in nature

Abstract

Negative frequency-dependent selection (NFDS) has been shown to maintain polymorphism in a diverse array of traits. The actionof NFDS has been confirmed through modeling, experimental approaches, and genetic analyses. In this study, we investigated NFDS in the wild using morph-frequency changes spanning a 20-year period from over 30 dimorphic populations of Datura wrightii. In these populations, plants either possess glandular (sticky) or non-glandular (velvety) trichomes, and the ratio of these morphs varies substantially among populations. Our method provided evidence that NFDS, rather than drift or migration, is the primary force maintaining this dimorphism. Most populations that were initially dimorphic remained dimorphic, and the overall mean and variance in morph frequency did not change over time. Furthermore, morph-frequency differences were not related to geographic distances. Together, these results indicate that neither directional selection, drift, or migration played a substantial role in determining morph frequencies. However, as predicted by negative frequency-dependent selection, we found that the rare morph tended to increase in frequency, leading to a negative relationship between the change in the frequency of the sticky morph and its initial frequency. In addition, we found that morph-frequency change over time was significantly correlated with the damage inflicted by two herbivores: Lema daturaphila and Tupiochoris notatus. The latter is a specialist on the sticky morph and damage by this herbivore was greatest when the sticky morph was common. The reverse was true for L. daturaphila, such that damage increased with the frequency of the velvety morph. These findings suggest that these herbivores contribute to balancing selection on the observed trichome dimorphism. K E Y W O R D S : balanced polymorphism, Datura wrightii, glandular trichomes, plant-herbivore interactions. Impact SummaryWe present a long-term observational study of morph frequency changes in naturally dimorphic populations of Datura wrightii. We were able to determine that negative frequency-dependent selection-rather than drift, migration, or directional selection-is the main contributor to the main-tenance of this dimorphism over the past 20 years. We also sampled herbivory across our sample of populations and found evidence suggesting that the damage inflicted by two species of specialist herbivores may underlie this selective regime.Negative frequency-dependent selection (NFDS)-a selective regime in which rare morphs are favored over common 8 3

Observational evidence of herbivore‐specific associational effects between neighboring conspecifics in natural, dimorphic populations of Datura wrightii

“…This extirpation has not been observed. Instead over the past two decades, the two morphs have continued to coexist (Goldberg et al., 2020). Taken together, our studies suggest two possibilities for why NFDS occurs over time among populations (i.e., the velvety morph increases when rare [Goldberg et al., 2020]), despite velvety plants receiving more damage when locally rare.…”

“…Instead over the past two decades, the two morphs have continued to coexist (Goldberg et al., 2020). Taken together, our studies suggest two possibilities for why NFDS occurs over time among populations (i.e., the velvety morph increases when rare [Goldberg et al., 2020]), despite velvety plants receiving more damage when locally rare. The first is that the scale at which we measured herbivory in this study was too small to capture the full extent of herbivory on the two trichome morphs within populations in our study system.…”

“…For example, herbivore populations often vary over the growing season of their hosts, and our visitation times (late April/early May for the spring 2018 visitation; late July/ early August for both summer measurements) may not correspond to the period in which these effects occur. It is also possible—given the degree to which herbivory varies from population to population (Goldberg et al., 2020)—that associational effects were occurring within some, but not all, of the populations we visited. In addition, the 1m scale at which we looked for associational effects may not match the scale upon which the processes underlying negative frequency‐dependent selection are playing out and previous studies have noted the importance of scale when assessing the roles of associational effects (Underwood et al., 2014).…”

“…For populations with fewer than 36 plants, all plants present were sampled. The population‐wide averages of these measurements were used in a prior study (Goldberg et al., 2020), but analyses of variation between individual plants in this dataset have not been previously presented.…”

“…These two morphs are easy to categorize by sight and touch in the field. Previous research using a statewide sample of populations has shown that this dimorphism is maintained by negative frequency‐dependent selection linked to two herbivorous insects (Goldberg et al., 2020). These two morphs do not produce significantly different herbivore‐induced volatile blends (Hare, 2007), but these blends do vary based upon the herbivore species (Hare & Sun, 2011).…”