Integrating evolutionarily novel horns within the deeply conserved insect head

David M Linz,Armin P Moczek

doi:10.1186/s12915-020-00773-9

Abstract

BackgroundHow novel traits integrate within ancient trait complexes without compromising ancestral functions is a foundational challenge in evo-devo. The insect head represents an ancient body region patterned by a deeply conserved developmental genetic network, yet at the same time constitutes a hot spot for morphological innovation. However, the mechanisms that facilitate the repeated emergence, integration, and diversification of morphological novelties within this body region are virtually unknown. Using horned Onthophagus beetles, we investigated the mechanisms that instruct the development of the dorsal adult head and the formation and integration of head horns, one of the most elaborate classes of secondary sexual weapons in the animal kingdom.ResultsUsing region-specific RNAseq and gene knockdowns, we (i) show that the head is compartmentalized along multiple axes, (ii) identify striking parallels between morphological and transcriptional complexity across regions, yet (iii) fail to identify a horn-forming gene module. Instead, (iv) our results support that sex-biased regulation of a shared transcriptional repertoire underpins the formation of horned and hornless heads. Furthermore, (v) we show that embryonic head patterning genes frequently maintain expression within the dorsal head well into late post-embryonic development, thereby possibly facilitating the repurposing of such genes within novel developmental contexts. Lastly, (vi) we identify novel functions for several genes including three embryonic head patterning genes in the integration of both posterior and anterior head horns.ConclusionsOur results illuminate how the adult insect head is patterned and suggest mechanisms capable of integrating novel traits within ancient trait complexes in a sex- and species-specific manner. More generally, our work underscores how significant morphological innovation in developmental evolution need not require the recruitment of new genes, pathways, or gene networks but instead may be scaffolded by pre-existing developmental machinery.

Highlights

How novel traits integrate within ancient trait complexes without compromising ancestral functions is a foundational challenge in evo-devo
We sought to test the hypothesis that the integration of novel traits within an ancestral trait complex requires the recruitment of additional genes and pathways into the gene networks instructing both within- and among-region development
While head horns constitute an evolutionary novelty, the patterning role of Wnt signaling discovered here may be more conserved: recent work by Magri et al shows that inhibiting Wnt signaling in the medial/dorsal head of adult Drosophila can expand the lateral compound eye into the medial/dorsal domain, resulting in a phenotype that parallels the expansion of the horn forming posterior region we have described here [31]

Summary

Introduction

How novel traits integrate within ancient trait complexes without compromising ancestral functions is a foundational challenge in evo-devo. The insect head represents an ancient body region patterned by a deeply conserved developmental genetic network, yet at the same time constitutes a hot spot for morphological innovation. The mechanisms that facilitate the repeated emergence, integration, and diversification of morphological novelties within this body region are virtually unknown. The developmental underpinnings of novel traits had to overcome multiple, interrelated challenges. To enable functional fine tuning by selection independent of other traits, novel traits needed to evolve developmental regulatory mechanisms with limited pleiotropic effects [2]. Novel traits had to find ways to integrate developmentally, physiologically, and morphologically, within and alongside preexisting structures without compromising their ancestral functions [4]. How novel traits achieve such integration within pre-existing contexts during ontogeny, and

Objectives

Methods

Results

Conclusion