Macroevolutionary Analyses Provide New Evidence of Phasmid Wings Evolution as a Reversible Process

Abstract

The concept that complex ancestral traits can never be recovered after their loss is still widely accepted, despite phylogenetic and molecular approaches suggest instances where phenotypes may have been lost throughout the evolutionary history of a clade and subsequently reverted back in derived lineages. One of the first and most notable examples of such a process is wing evolution in phasmids; this polyneopteran order of insects, which comprises stick and leaf insects, has played a central role in initiating a long-standing debate on the topic. In this study, a novel and comprehensive time tree including over 300 Phasmatodea species is used as a framework for investigating wing evolutionary patterns in the clade. Despite accounting for several possible biases and sources of uncertainty, macroevolutionary analyses consistently revealed multiple reversals to winged states taking place after their loss, and reversibility is coupled with higher species diversification rates. Our findings support a loss of or reduction in wings that occurred in the lineage leading to the extant phasmid most recent common ancestor, and brachyptery is inferred to be an unstable state unless co-opted for nonaerodynamic adaptations. We also explored how different assumptions of wing reversals probability could impact their inference: we found that until reversals are assumed to be over 30 times more unlikely than losses, they are consistently inferred despite uncertainty in tree and model parameters. Our findings demonstrate that wing evolution is a reversible and dynamic process in phasmids and contribute to our understanding of complex trait evolution. [Dollo’s law; Phasmatodea; phylogenetic comparative methods; polyneoptera; reversals; wing.]

Cladomorphus petropolisensis, a New Species of Stick Insect from the Atlantic Forest, Rio de Janeiro, Brazil

“…Nevertheless, molecular approaches have been of great importance to delimit distinct independent evolutionary unities, not just in that group, but also in several insect orders [ 36 , 37 , 38 , 39 ]. DNA sequences have been commonly and recently used to recover the higher-level phylogenetic relationships of phasmids [ 5 , 40 , 41 , 42 , 43 , 44 , 45 ]. However, it has been more scarcely used in an integrative taxonomy context to help species delimitation [ 46 , 47 ].…”

Phasmid species that inhabit colder environments are less likely to have the ability to fly

“…Based on some estimates, approximately half of the species lack wings and are therefore incapable of flight (Zeng et al, 2020). Moreover, the evolution of flight in phasmids is thought to be fairly labile, with multiple evolutionary transitions between nonflying and flying states (Bank & Bradler, 2022; Forni et al, 2022; Whiting et al, 2003). The direction of these evolutionary transitions is debated.…”

“…The direction of these evolutionary transitions is debated. Some hypothesize that flight was lost multiple times (Stone & French, 2003; Trueman et al, 2004), while others hypothesize that flight was reacquired multiple times (Bank & Bradler, 2022; Forni et al, 2022; Whiting et al, 2003). Importantly, while the flight evolution hypotheses discussed above were originally proposed to explain the evolution of flight loss, they can also be expanded to include the re‐evolution of flight.…”

Beyond winglets: evolutionary scaling of flight-related morphology in stick insects (Phasmatodea)

“…1C ). The size of phasmid wings (and presumably flight capability) show complex phylogenetic patterns, and recent work suggests both flight gains and losses (Bank et al, 2021; Bank and Bradler, 2022; Forni et al, 2022). In general, relaxed selection for flight may underpin various partial-winged morphologies within an arboreal context.…”

“…Current evidence suggests two ‘adaptive peaks’ associated with either large or miniaturized wings, which are evolutionary consequences of both gains and reductions of flight over various evolutionary timescales ( Fig. 1D ) (Zeng et al, 2020; Forni et al, 2022).…”