Fruit odorants mediate co-specialization in a multispecies plant–animal mutualism

Abstract

Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats ( Carollia spp.) and plants ( Piper spp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models in Piper . Through behavioural assays, we found Carollia prefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of two Piper species highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropical Piper fruits evolved in tandem with seed dispersal by scent-oriented Carollia bats. Specifically, fruit scent chemistry in some Piper species fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent in Piper , our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity.

Variation in ripe fruit volatiles across the tomato clade: An evolutionary framework for studying fruit scent diversity in a crop wild relative

“…In line with this hypothesis, VOCs are important for attracting nonhuman seed dispersers and signaling fruit ripeness (Nevo and Ayasse, 2019). Evidence that fruit scent chemicals evolved in tandem with consumption by animal dispersers has come from recent work on frugivorous bats (Hodgkison et al, 2013; Santana et al, 2021) and lemurs (Nevo et al, 2018). A mechanism underlying this fruit–frugivore coevolution could be that fruit scent communicates an honest signal of internal nutrient content to potential animal consumers (Nevo et al, 2019, 2020a).…”

“…Additionally, fruit scent may be constrained by non‐adaptive chemical, developmental, or phylogenetic limitations on VOC production (Nevo et al, 2020b). The degree of phylogenetic constraint, or conservatism (i.e., similarity due to inheritance from common ancestors), appears to differ depending on the system, with some multi‐genera community‐based studies not finding much conservatism (Nevo et al, 2018, 2020b) and other narrower lineage‐focused studies either finding it in Ficus (Hodgkison et al, 2013) or not finding it in Piper (Santana et al, 2021). Despite recent interest in wild fruit VOCs, the field is still young, and data only exists for a small number of non‐agricultural systems.…”

Biotic and abiotic factors shaping bat activity in Maryland soybean fields

“…Some have posited that insectivorous bats do not use olfaction to forage (Bloss, 1999); however, to our knowledge, no previous study has specifically tested this hypothesis. In contrast, frugivorous and nectivorous bat species clearly rely on olfaction, in addition to echolocation, to detect plant chemical cues and locate preferred food sources, such as ripe fruits (Santana et al, 2021; Thies et al, 1998) or nectar‐filled flowers (Gonzalez‐Terrazas et al, 2016). Frugivorous and nectivorous bats are direct plant mutualists, serving as seed dispersers and pollinators, and plants emit chemical cues that facilitate or encourage this foraging behavior.…”

Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical bats

“…Thus, in combination with numerous unique volatile compounds emitted by these plant resources (Santana et al. 2021 ), we expect that molecular and morphological signatures of olfactory adaptation to plant visiting should be detectable. Similar trends have been noted in insects (Dekker et al.…”

“…Behavioral experiments of some plant-visiting noctilionoids have demonstrated they primarily rely on olfaction and that echolocation is supplemental (Thies et al 1998;Gonzalez-Terrazas et al 2016;Leiser-Miller et al 2020;Brokaw et al 2021), and there is little variation in echolocation frequency among phyllostomids (Gessinger et al 2021). Thus, in combination with numerous unique volatile compounds emitted by these plant resources (Santana et al 2021), we expect that molecular and morphological signatures of olfactory adaptation to plant visiting should be detectable. Similar trends have been noted in insects (Dekker et al 2006;Brand et al 2015).…”