Plasticity of mycangia in Xylosandrus ambrosia beetles

Abstract

Insects that depend on microbial mutualists evolved a variety of organs to transport the microsymbionts while dispersing. The ontogeny and variability of such organs is rarely studied, and the microsymbiont's effects on the animal tissue development remain unknown in most cases. Ambrosia beetles (Coleoptera: Curculionidae: Scolytinae or Platypodinae) and their mutualistic fungi are an ideal system to study the animal-fungus interactions. While the interspecific diversity of their fungus transport organ-mycangia-is well-known, their developmental plasticity has been poorly described. To determine the ontogeny of the mycangium and the influence of the symbiotic fungus on the tissue development, we dissected by hand or scanned with micro-CT the mycangia in various developmental stages in five Xylosandrus ambrosia beetle species that possess a large, mesonotal mycangium: Xylosandrus amputatus, Xylosandrus compactus, Xylosandrus crassiusculus, Xylosandrus discolor, and Xylosandrus germanus. We processed 181 beetle samples from the United States and China. All five species displayed three stages of the mycangium development: (1) young teneral adults had an empty, deflated and cryptic mycangium without fungal mass; (2) in fully mature adults during dispersal, the pro-mesonotal membrane was inflated, and most individuals developed a mycangium mostly filled with the symbiont, though size and symmetry varied; and (3) after successful establishment of their new galleries, most females discharged the bulk of the fungal inoculum and deflated the mycangium. Experimental aposymbiotic individuals demonstrated that the pronotal membrane invaginated independently of the presence of the fungus, but the fungus was required for inflation. Mycangia are more dynamic than previously thought, and their morphological changes correspond to the phases of the symbiosis. Importantly, studies of the fungal symbionts or plant pathogen transmission in ambrosia beetles need to consider which developmental stage to sample. We provide illustrations of the different stages, including microphotography of dissections and micro-CT scans.

Micro-computed tomography permits enhanced visualization of mycangia across development and between sexes in Euwallacea ambrosia beetles

“…should start exploring the genetic underpinnings of mycangial development and 2) the direct physical contact with their symbiotic fungi may not be required to induce mycangial development, similar to what has been shown for mesonotal mycangia in Xylosandrus ambrosia beetles (Li et al 2019) [37].…”

Structure of the Ambrosia Beetle (Coleoptera: Curculionidae) Mycangia Revealed Through Micro-Computed Tomography

“…All beetles had previously been collected using alcohol-baited traps that capture flying beetles. This was intentional because the mycangia of ambrosia beetles are most developed during the beetle’s flight dispersal stage ( Li et al 2018 ). Specimens were preserved in 95% ethanol prior to treatment and identified with the aid of a stereomicroscope using the most recent taxonomic literature for the group ( Beaver and Gebhardt 2006 , Rabaglia et al 2006 , Gomez et al 2018 ).…”

“…It is often utilized to image dry samples of approximately 1~200 mm in length, although it is capable of obtaining a resolution down to approximately 0.1 μm, permitting the study of smaller structures (of less than 1 μm in length). Several studies have already shown the potential of micro-CT techniques to deliver novel data for investigating functional morphology in beetles ( Li et al 2011 , van de Kamp et al 2011 , Wilhelm et al 2011 , Hörnschemeyer et al 2013 , Li et al 2018 ). Paraffin sections have been utilized for about 150 yr ( Van den Tweel and Taylor 2010 ), and with improved stains and tissue processors, this method remains in extensive use in biology and medicine to this day ( Titford 2006 ).…”

Seasonal changes in population structure of the ambrosia beetle Xylosandrus compactus and its associated fungi in a southern Mediterranean environment

“…Skelton et al [47] demonstrated that closely related symbionts are interchangeable by offering alternative fungal symbionts from different Ambrosiella clade in experimental galleries inoculated with X. compactus. However, Li et al [48] showed that aposymbiotic specimens, deprived of Ambrosiella, in any case develop empty mycetangia.…”

“…compactus . However, Li et al [ 48 ] showed that aposymbiotic specimens, deprived of Ambrosiella , in any case develop empty mycetangia.…”