Abstract
With fossil representatives from the Silurian capable of respiring atmospheric oxygen, millipedes are among the oldest terrestrial animals, and likely the first to acquire diverse and complex chemical defenses against predators. Exploring the origin of complex adaptive traits is critical for understanding the evolution of Earth’s biological complexity, and chemical defense evolution serves as an ideal study system. The classic explanation for the evolution of complexity is by gradual increase from simple to complex, passing through intermediate “stepping stone” states. Here we present the first phylogenetic-based study of the evolution of complex chemical defenses in millipedes by generating the largest genomic-based phylogenetic dataset ever assembled for the group. Our phylogenomic results demonstrate that chemical complexity shows a clear pattern of escalation through time. New pathways are added in a stepwise pattern, leading to greater chemical complexity, independently in a number of derived lineages. This complexity gradually increased through time, leading to the advent of three distantly related chemically complex evolutionary lineages, each uniquely characteristic of each of the respective millipede groups.
Highlights
One of the most significant events in the evolution of early life on planet Earth took place in the middle Silurian —roughly 423 million years ago— with the origin of the first land animals[1,2], triggering the greatest documented expansion of species-level diversity[3]
Studies focusing on patterns of chemical production in millipedes have led to the same hypothesis[20,24], but in the absence of a well-sampled phylogenetic framework, proper ancestral character mapping methods and models of character evolution
Based on a newly derived phylogenetic framework and a synthesis of all the chemical data available to us at this time, the main goal of our study is to test the hypothesis of step-wise evolution from simple to complex[8,9,10] in arthropod chemical defense systems using a phylogenetic comparative approach by asking (i) did benzoquinone and cyanogenic production evolve after the ability to produce phenols in eugnathan millipedes and (ii) were the benzoquinone defense systems produced in a step-wise fashion from simple to complex?
Summary
One of the most significant events in the evolution of early life on planet Earth took place in the middle Silurian —roughly 423 million years ago— with the origin of the first land animals[1,2], triggering the greatest documented expansion of species-level diversity[3]. We investigate the evolution of complex chemical defense systems in the arthropod class Diplopoda (millipedes) using an interdisclipinary approach that employs analytical chemistry and modern genomics-based approaches to generate an evolutionary, phylogenetic framework to investigate chemical defense evolution across earth’s oldest known terrestrial animal group. All but five millipede orders have repugnatorial glands that secrete chemical defenses when disturbed by predators[19] These chemicals belong to at least eight molecule types (i.e., 1,4-benzoquinones, phenols, hydrogen cyanide, quinazolinones, and alkaloids, see Fig. 2)[20]. Molecular phylogenetic analyses have generated some surprising results, including the paraphyly of Nematophora, and the placement of Stemmiulida as sister to Polydesmida[15,27] These past results have key implications for understanding chemical evolution, suggesting that, because of their near-universality in Eugnatha, phenolic compounds are the oldest defense chemicals produced by eugnathan millipedes. The conflict between morphological and traditional (Sanger-based) molecular data provides little in the way of reliable answers to some of these long-established evolutionary questions
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