Master of mimicry : “chameleon vine” and its Mimetic Polymorphism

Boquila trifoliolata

Boquila trifoliolata is a woody vine with a highly variable appearance due to its crypsis abilities. The vines are evergreen or partly deciduous, meaning they largely retain their leaves over winter. The vines follow a twining pattern when climbing host plants, meaning the stems bend around host plants during their ascent. The branches are thin, less than 1 cm (0.39 in) in diameter, and are covered in red-brown bark. The lenticels are elliptical in shape, and the wider branches are a speckled grey color. When not mimicking a host plant, B. trifoliata employs smaller 'charlatan leaves' that are short, stubby, and have three lobes (trifoliate).

Boquila trifoliolata is the only plant known to engage in mimetic polymorphism, meaning it can mimic the leaves of multiple host plants. Other species of vines are capable of limited crypsis for one host species, but B. trifoliata is notable since it can mimic the leaves of multiple species, with one vine capable of simultaneously mimicking multiple hosts. Mimetic polymorphism is only observed elsewhere in some species of butterflies, but that is the result of genetic divergence, unlike B. trifoliata which engages in rapid changes in leaf morphology.

Once the vines approach a host tree's branches, the leaves begin to change their size, shape, colour, vein patterns, spines, and orientation to match the host plant; sometimes expanding to 10x their original size. B. trifoliata has been observed mimicking over 20 different species of plants.

Boquila is a genus of flowering plants in the family Lardizabalaceae, endemic to temperate forests of central and southern Chile and Argentina. It is monotypic, being represented by the single species Boquila trifoliolata, locally known as voqui blanco or pilpil in its native range, and sometimes referred as the 'chameleon vine' since a recent report on leaf mimicry.

Unlike most other mimicking species, close proximity is enough to induce mimicry and contact is not required. In one controversial study, B. trifoliata has been noted to mimic the leaves of plastic plants. If the vines approach another tree, the vine begins simultaneously mimicking that species as well. Mimicry is largely confined to the leaves closest to the host, meaning that sections of the vine approximately 60 cm (24 in) away from the host retain the non-mimicking phenotype. This is a form of Batesian mimicry,  where the B. trifoliata is harmless but resembles a less palatable or harmful plant to ward off herbivory species and pests.

The species was first described in 1782 by Juan Ignacio Molina, and the genus itself was established in 1839 by Joseph Decaisne. B. trifoliata forms non-parasitic vines that wind around host plants, using them for structure and protection. B. trifoliata is monoecious, and its flowers are an off white color. It bears an edible fruit and has been historically used in rope and basket making.

B. trifoliata is the only known plant species reported to engage in mimetic polymorphism, or the ability to mimic multiple host species, often simultaneously. This is a form of Batesian mimicry, when a harmless species mimics a harmful one to ward off predators. Contact between the vines and host trees was reported not to be necessary for mimicking to commence. However, after a decade of the original study describing the species mimicry capabilities in 2014, no independent research groups have verified the field observations and the mechanism by which this mimicry would occur is still unknown.

Believe it or not, all the above leaves are from the same species of plant. Boquila’s mind-blowing ability is that its leaves change shape to mimic those of the nearest trees. Somehow, their size, shape, stalk and colour morph to blend in with nearby tree leaves, disguising themselves from animals which might eat them.

They can even grow spiny tips on the leaves should the host plant have such spines, and can mimic different types of foliage on the same individual plant. On any one Boquila trifoliolata plant, some leaves might be 10 times the size of others.

But this of course begs the question - how on Earth does it “know” which leaves to mimic? It can’t be by touch, because it doesn’t even require physical contact to mimic.

Hypotheses about the mimicry mechanism include microbial mediated horizontal gene transfer, volatile organic compound sensing, and the use of eye-like structures.

The exact mechanism by which mimicry occurs is not well studied but may involve chemical, odour, genetic, metagenomic, transcriptomic, proteomic, metabolomic, epigenetic, and/or microbial cues to identify and mimic the species it is attached to.

Various theories that are being considered:

Volatile organic compounds
Plant ecologist Ernesto Gianoli proposed that the host tree may be emitting volatile organic compounds (VOCs) into the environment that B. trifoliata can detect.The use of VOC-mediated plant-to-plant communication is widely employed in non-specific biological processes, including up-regulation of defense-related genes, and could explain why no contact is necessary for mimicry. Criticisms of this hypothesis are that this would mark the first time that VOCs were used to change plant morphology, and that B. trifoliata's mimicry has a level of specificity that is not normally seen with VOC-mediated responses.

Horizontal gene transfer
Another hypothesis proposed by Gianoli is that B. trifoliata's mimicry is mediated by endophytic microbes that conduct horizontal gene transfer (HGT) between B. trifoliata and the host plant. This would influence the genes, transposons, and/or epigenetics of the plant's leaves, identifying the host and changing the leaf's morphology without necessitating physical contact. In a 2021 study, Gianoli found that the microbiomes of B. trifoliata and its host plant show significant overlap following the initiation of mimicry. Gianoli has argued this could represent a mechanism behind B. trifoliata's mimicry but still acknowledged that there are limitations to this hypothesis. While HGT commonly occurs between different species, it takes many years and manifests in discrete events. Additionally, HGT between plants is most commonly observed in cases of parasitism, which B. trifoliata does not engage in.

Ocelli
In a 2021 study published in the journal Plant Signaling & Behavior, Felipe Yamashita and Jacob White claimed that B. trifoliata may employ a primitive form of vision to identify and mimic their hosts. This hypothesis is based upon 1905 and 1907 claims by Gottlieb Haberlandt and Francis Darwin, respectively, that some plants use 'ocelli' or lens-like cells to focus light onto other light sensitive cells. In this study, B. trifoliata was observed mimicking the leaf shapes of plastic plants, and researchers refined Haberlandt and Darwin's ocelli hypothesis, claiming that B. trifoliata may be using convex shaped lenses in epidermal tissue that can detect light and "see" the shapes of nearby leaves. They further proposed that, B. trifoliata processes that information through an unknown means, possibly through neuron-like structures in order to initiate mimicry. The study also found that non-mimetic leaves have more free-end veinlets and identified the hormone auxin as a possible mediator in changes to leaf morphology.

This paper received substantial media coverage, was praised by F1000's Faculty Opinions, and went viral on some of the social media platforms  following its release. Plant biologist and Plant Signaling and Behavior's editor-in-chief, František Baluška praised this hypothesis, and claimed that root skototropism and photoreceptive cells in algae were analogous mechanisms for "plant sight". However, the paper's conclusions have largely been met with skepticism by scientists. Criticisms of the paper include poor methodology, White's lack of a scientific background, and possible conflicts of interest between Baluška and Yamashita.