Microorganisms in the reproductive tissues of arthropods

Abstract

Microorganisms that reside within or transmit through arthropod reproductive tissues have profound impacts on host reproduction, health and evolution. In this Review, we discuss select principles of the biology of microorganisms in arthropod reproductive tissues, including bacteria, viruses, protists and fungi. We review models of specific symbionts, routes of transmission, and the physiological and evolutionary outcomes for both hosts and microorganisms. We also identify areas in need of continuing research, to answer the fundamental questions that remain in fields within and beyond arthropod-microorganism associations. New opportunities for research in this area will drive a broader understanding of major concepts as well as the biodiversity, mechanisms and translational applications of microorganisms that interact with host reproductive tissues.

Figure 1.. Example microorganisms associated with arthropod reproductive tissues.

The silhouette is a representative image that includes organs from both males and females, as well as various species of insects, and is therefore not anatomically accurate for any given arthropod species, and neither is it to scale to enable visualization of all organs. Select microorganisms and viruses are listed in their primary or additional densely populated body sites. The list is not comprehensive of all symbionts, all tissue localizations, or all functions, but represents many known symbioses. In addition, symbionts may not be present in the same tissues or exhibit the same phenotypes in every strain or host. The microorganisms that are listed under the ‘gut, hemolymph and fat body’ as well as the ‘bacteriome or mycetome’ are present in both sexes of some species and are included because all contact reproductive tissues at some point (typically during transmission) even though they primarily or often reside in other tissues. The function is listed as “unknown phenotype or function” if the presence of the symbiont is known, but the effect on the arthropod host is not well established. In addition, a function of a symbiont may only apply in some circumstances (for example, different hosts or strains).

Figure 2.. Transmission routes of microorganisms in the reproductive tract in arthropods.

Depicted are representative methods for transmission of microorganisms in the reproductive tract between individuals. Pink circles represent symbionts, and pink outlines or coatings indicate outer coverage by symbionts. a) Horizontal transmission can spread microorganisms between reproductive tissues of different host individuals, usually through copulation. b) Certain hereditary microorganisms can be vertically transmitted from mother to offspring via the milk glands, as has been reported for the tsetse fly symbiont Wigglesworthia glossinidia. c) Hereditary endosymbionts, including many common reproductive parasites, can be vertically transmitted via infection in the ovarian tissues and passage internally to embryos. d) Bacteria in specialized organs can be smeared onto embryos as they are laid so that offspring are coated with the microorganisms when they eclose. e) Hereditary symbionts may be acquired post egg-laying through various mechanisms, including passage through symbiont capsules during eclosion. f) Microorganisms may be paternally transmitted via various mechanisms, including packaging within sperm heads that enables infection of offspring. G) Certain microorganisms may also be cyclically transmitted through both insect and plant hosts. The insects often carry these microorganisms on their genitalia and can pass them sexually to other insects, horizontally to new plants or vertically to offspring.

Figure 3.. Effects on the genomes and transcriptomes of hosts and microorganisms.

Post-symbiosis sections demonstrate population-level changes many generations since pre-symbiosis. Each effect is not universal to all symbioses and instead represents changes known in some systems. The top panel shows changes that can occur in host DNA, where there can be epigenetic alterations, changes in gene expression in the presence of symbionts, fewer mitochondrial DNA haplotypes in the population, and horizontal gene transfer from microbe to host. The bottom panel shows changes that can occur in microbial DNA, where there can be accelerated gene evolution, increased AT content, horizontal gene transfer from host to microbe, and an overall reduced genome size.