The Life of an Insect Endosymbiont from the Cradle to the Grave

Abstract

Host-beneficial endosymbioses, which are formed when a microorganism takes up residence inside another cell and provides a fitness advantage to the host, have had a dramatic influence on the evolution of life. These intimate relationships have yielded the mitochondrion and the plastid (chloroplast) -the ancient organelles that in part define eukaryotic life -along with many more recent associations involving a wide variety of hosts and microbial partners. These relationships are often envisioned as stable associations that appear cooperative and persist for extremely long periods of time. But recent evidence suggests that this stable state is often born from turbulent and conflicting origins, and that the apparent stability of many beneficial endosymbiotic relationships -although certainly real in many cases -is not an inevitable outcome of these associations. Here we review how stable endosymbioses form, how they are maintained, and how they sometimes break down and are reborn. We focus on relationships formed by insects and their resident microorganisms because these symbioses have been the focus of significant empirical work over the last two decades. We review these relationships over five life stages: origin, birth, middle age, old age, and death.

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

“…Only extensive HT of Coxiella ‐LE among tick genera may explain these phylogenetic incongruences. Because facultative, but not obligate, symbionts can undergo HT between host species (Bennett & Moran, ; McCutcheon et al, ; Moran et al, ; Wernegreen, ), this suggests that some Coxiella ‐LE are facultative symbionts of ticks. Interestingly, Coxiella ‐LE is a facultative symbiont in some Ixodes species, such as I. ricinus and I. uriae (Duron et al, , ; Duron, Jourdain, & McCoy, ).…”

“…Indeed, ancestral Coxiella ‐LE may have evolved overly reduced (degraded) genomes and become maladapted, opening the road to replacement by a new symbiont. This degeneration–replacement model has been proposed for other arthropods such as cicadas (Campbell et al, ; Łukasik et al, ; Matsuura et al, ), but replacements are expected to be transient making them difficult to observe (McCutcheon et al, ). In Amblyomma , the observations of three species with co‐infections by ancestral Coxiella ‐LE and recently acquired Francisella ‐LE may correspond to this transient state before extinction of Coxiella ‐LE.…”

“…Arthropods and beneficial maternally inherited symbionts can form evolutionarily stable associations lasting for millions of years, but that are not necessarily permanent (Bennett & Moran, 2015;McCutcheon, Boyd, & Dale, 2019;Moran et al, 2008;Wernegreen, 2012). Recent phylogenetic reconstructions suggest that beneficial symbiotic relationships can break down: recently acquired symbionts can replace ancestral beneficial symbionts and provide similar benefits to the host (McCutcheon et al, 2019;Sudakaran, Kost, & Kaltenpoth, 2017). An alternative scenario is that recently acquired symbionts may cooperate with ancestral beneficial symbionts (Moran et al, 2008;Vautrin & Vavre, 2009).…”

“…The functions of ancestral beneficial symbionts may be complemented by recently acquired cosymbionts and their coexistence can be ultimately stable over millions of years (Meseguer et al, 2017). New beneficial symbionts often originate from microbes that are abundant in the host environment, potentially including entomopathogens, parasites vectored by arthropods or other maternally inherited symbionts, primarily facultative (i.e., not essential) for host survival (Koga & Moran, 2014;Matsuura et al, 2018;McCutcheon et al, 2019;Sachs, Skophammer, & Regus, 2011). These facultative symbionts, however, determine important traits in arthropods: protection against natural enemies, adaptation to changing environments or reproductive traits (Engelstädter & Hurst, 2009;Ferrari & Vavre, 2011;Moran et al, 2008;Oliver et al, 2003).…”

Repeated evolution of bacteriocytes in lygaeoid stinkbugs

“…Thus, we speculate that this type of behavioural adaptation might have occurred after or before the evolution of bacteriocytes, and the following inaccessibility to specific groups of soil bacteria could have caused the complete loss of gut symbioses in certain lygaeoid taxa. We also speculate that bacterial factors such as secretion systems or quorum sensing of Sodalis-like symbionts in ancestral lygaeoid bugs might have played roles in the acquisition of bacteriocytes at the nascent stage of symbiosis, so it is worth comparing these mechanisms along with the evolution of bacteriocyte-associated symbioses found in diverse insects (Dale et al, 2001;Akman et al, 2002;Gil et al, 2003;Fukatsu et al, 2007;Clayton et al, 2012;Toju et al, 2013;Oakeson et al, 2014;Nováková et al, 2015;Husnik and McCutcheon, 2016;Enomoto et al, 2017;McCutcheon et al, 2019).…”