Biogeography confounds the signal of cospeciation in Batesian mimicry

Abstract

Since the inception of the field of evolution, mimicry has yielded insights into foundational evolutionary processes, including adaptive peak shifts, speciation, and the emergence and maintenance of phenotypic polymorphisms.^1,2,3 In recent years, the coevolutionary processes generating mimicry have gained increasing attention from researchers. Despite significant advances in understanding Batesian and Müllerian mimicry in Lepidopteran systems, few other mimetic systems have received similar detailed research. Here, we present a Batesian mimicry complex involving flightless, armored Pachyrhynchus weevils and their winged Doliops longhorn beetle mimics and examine their coevolutionary patterns within the Philippine archipelagos. Pachyrhynchus weevils are primarily found in the Philippines, where distinct species radiations have occurred on different islands, each with unique color patterns serving as a warning to predators. This defensive trait and mimicry between unrelated species were first described by Wallace in 1889. Notably, the distantly related longhorn beetle Doliops, despite being soft-bodied and ostensibly palatable, mimics the heavily armored, flightless Pachyrhynchus. To address mimicry in this system, we reconstructed the phylogeny of Doliops using a probe set consisting of 38,000 ultraconserved elements. Our study examines the following questions central to understanding the Pachyrhynchus-Doliops mimicry system: (1) to what extent are coevolutionary interactions conserved (i.e., lineage-constrained) and (2) are the codiversification patterns primarily driven by biotic or abiotic factors?^4,5,6 To assess color mimicry and cospeciation, we examined the evolution of nanostructure-based warning colors and the effect of island biogeography on cospeciation. Our findings demonstrate the beetle's ability to repeatedly evolve multiple solutions to similar evolutionary challenges, evolving similar color patterns using different types of photonic crystals with varying degrees of order. We revealed that the observed pattern of cospeciation is driven mainly by abiotic factors from their biogeographic history. Unlike the patterns of coevolution seen between angiosperms and insect lineages,⁷ most ecological interactions do not persist longer than a few million years, leading to patterns of modularity rather than ecological nestedness.^4,6,7.

Keywords: Coleoptera; Pachyrhynchus; coevolution; cospeciation; insect nanostructure; island biogeography; mimicry; photonic crystal; phylogenomic.