Description of the basic features of parent-offspring stomodeal trophallaxis in the subsocial wood-feeding cockroach Salganea esakii (Dictyoptera, Blaberidae, Panesthiinae)

Shimada, Keisuke; Maekawa, Kazuyuki

doi:10.1111/j.1479-8298.2010.00406.x

Cited by 14 publications

(7 citation statements)

References 13 publications

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“…Like many animals, omnivorous cockroaches are thought to obtain their gut microbiota via the environment rather than via vertical transmission. However, their typically gregarious lifestyles offer extensive opportunities for insect-to-insect transmission through coprophagy and trophallaxis (39)(40)(41)(42)(43). Insect-to-insect transmission is likely particularly important for the acquisition of oxygen-sensitive Firmicutes and Bacteroidetes, which are also among the most abundant members of the cockroach gut microbiota.…”

Section: Discussionmentioning

confidence: 99%

Phylosymbiosis across Deeply Diverging Lineages of Omnivorous Cockroaches (Order Blattodea)

Tinker

Ottesen

2020

Appl Environ Microbiol

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The gut microbiome is shaped by both host diet and host phylogeny. However, separating the relative influence of these two factors over long periods of evolutionary time is often difficult. We conducted a 16S rRNA gene amplicon-based survey of the gut microbiome from 237 individuals and 19 species of omnivorous cockroaches from the order Blattodea. The order Blattodea represents an ancient lineage of insects that emerged over 300 million years ago, have a diverse gut microbiota, and have a typically gregarious lifestyle. All cockroaches shared a broadly similar gut microbiota, with 66 microbial families present across all species and 13 present in every individual examined. Although our network analysis of the cockroach gut microbiome showed a large amount of connectivity, we demonstrated that gut microbiota cluster strongly by host species. We conducted follow-up tests to determine if cockroaches exhibit phylosymbiosis, or the tendency of host-associated microbial communities to parallel the phylogeny of related host species. Across the full data set, gut microbial community similarity was not found to correlate with host phylogenetic distance. However, a weak but significant phylosymbiotic signature was observed using the matching cluster metric, which allows for localized changes within a phylogenetic tree that are more likely to occur over long evolutionary distances. This finding suggests that host phylogeny plays a large role in structuring the cockroach gut microbiome over shorter evolutionary distances and a weak but significant role in shaping the gut microbiome over extended periods of evolutionary time. IMPORTANCE The gut microbiome plays a key role in host health. Therefore, it is important to understand the evolution of the gut microbiota and how it impacts, and is impacted by, host evolution. In this study, we explore the relationship between host phylogeny and gut microbiome composition in omnivorous, gregarious cockroaches within the Blattodea order, an ancient lineage that spans 300 million years of evolutionary divergence. We demonstrate a strong relationship between host species identity and gut microbiome composition and found a weaker but significant role for host phylogeny in determining microbiome similarity over extended periods of evolutionary time. This study advances our understanding of the role of host phylogeny in shaping the gut microbiome over different evolutionary distances.

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Section: Discussionmentioning

confidence: 99%

Phylosymbiosis across Deeply Diverging Lineages of Omnivorous Cockroaches (Order Blattodea)

Tinker

Ottesen

2020

Appl Environ Microbiol

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“…Like Cryptocercus, Salganea lives in a system of galleries and chambers chewed into rotten wood, and exhibits long term, biparental care that includes the defense and feeding of young nymphs. Early instars periodically cling to the mouthparts of a parent and take liquids via oral feeding (Shimada and Maekawa 2011). Young nymphs of Salganea closely resemble those of Cryptocercus; they have reduced eyes and a transparent, unpigmented cuticle.…”

Section: Size Shift #1: Eggs/neonates In Subsocial Ancestorsmentioning

confidence: 99%

Body Size and Termite Evolution

Nalepa

2011

Evol Biol

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Termites are a monophyletic lineage within the paraphyletic Blattaria, with xylophagous cockroaches in the genus Cryptocercus as sister group. Given this ancestry, termite divergence involved a substantial leap in body plans, as they are pale, fragile, and miniaturized relative to most cockroaches. Here I suggest that the evolutionary transition to an altricial morphotype in termites is grounded in the economics of utilizing a wood diet, and occurred via a series of sequential steps associated with modifications in social behavior. The chief benefit of an altricial morphotype is suggested to be nitrogen made available by decreasing individual body size and by dispensing with a heavy, melanized cuticle. The primary costs lie in increased vulnerability to environment hazards, including predators, pathogens, and desiccation. Termites tipped the evolutionary scale via cooperative behaviors that mitigate the cost or amplify the benefit of a small, fragile morphotype, and were present in rudimentary form in their cockroach relatives. These include building behavior, cooperative feeding, allogrooming, and most notably, trophallaxis. It was the directed circulation of nitrogenous reserves via trophallactic feeding among units of the superorganism rather than their progressive storage in a large, heavily armored body that was the foundation of termite evolutionary success.

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“…Wood roaches of the genus Salganea , for example, have evolved morphological adaptations of the mouthparts to facilitate the uptake of stomodeal substances via trophallaxis by the mother [ 16 – 18 ]. However, it is currently unclear whether these substances contain wood fragments, nutrients, and/or enzymes or other chemicals involved in the degradation of cellulose [ 19 ]. Generally, oral fluids exchanged by trophallaxis may include proteins that are regulators of growth, development, and behavioural maturation [ 20 , 21 ].…”

Section: Introductionmentioning

confidence: 99%

Offspring dependence on parental care and the role of parental transfer of oral fluids in burying beetles

et al. 2018

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BackgroundImmature stages of many animals can forage and feed on their own, whereas others depend on their parents’ assistance to obtain or process food. But how does such dependency evolve, and which offspring and parental traits are involved? Burying beetles (Nicrophorus) provide extensive biparental care, including food provisioning to their offspring. Interestingly, there is substantial variation in the reliance of offspring on post-hatching care among species. Here, we examine the proximate mechanisms underlying offspring dependence, focusing on the larvae of N. orbicollis, which are not able to survive in the absence of parents. We specifically asked whether the high offspring dependence is caused by (1) a low starvation tolerance, (2) a low ability to self-feed or (3) the need to obtain parental oral fluids. Finally, we determined how much care (i.e. duration of care) they require to be able to survive.ResultsWe demonstrate that N. orbicollis larvae are not characterized by a lower starvation tolerance than larvae of the more independent species. Hatchlings of N. orbicollis are generally able to self-feed, but the efficiency depends on the kind of food presented and differs from the more independent species. Further, we show that even when providing highly dependent N. orbicollis larvae with easy ingestible liquefied mice carrion, only few of them survived to pupation. However, adding parental oral fluids significantly increased their survival rate. Finally, we demonstrate that survival and growth of dependent N. orbicollis larvae is increased greatly by only a few hours of parental care.ConclusionsConsidering the fact that larvae of other burying beetle species are able to survive in the absence of care, the high dependence of N. orbicollis larvae is puzzling. Even though they have not lost the ability to self-feed, an easily digestible, liquefied carrion meal is not sufficient to ensure their survival. However, our results indicate that the transfer of parental oral fluids is an essential component of care. In the majority of mammals, offspring rely on the exchange of fluids (i.e. milk) to survive, and our findings suggest that even in subsocial insects, such as burying beetles, parental fluids can significantly affect offspring survival.

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Description of the basic features of parent-offspring stomodeal trophallaxis in the subsocial wood-feeding cockroach Salganea esakii (Dictyoptera, Blaberidae, Panesthiinae)

Cited by 14 publications

References 13 publications

Phylosymbiosis across Deeply Diverging Lineages of Omnivorous Cockroaches (Order Blattodea)

Phylosymbiosis across Deeply Diverging Lineages of Omnivorous Cockroaches (Order Blattodea)

Body Size and Termite Evolution

Offspring dependence on parental care and the role of parental transfer of oral fluids in burying beetles

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