Microbiome-assisted carrion preservation aids larval development in a burying beetle

Shukla, Shantanu; Plata, Camila; Reichelt, Michael; Steiger, Sandra; Heckel, David G.; Kaltenpoth, Martin; Vilcinskas, Andreas; Vogel, Heiko

doi:10.1073/pnas.1812808115

Cited by 97 publications

(118 citation statements)

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“…This thermoregulation strategy probably involves microbial activity. Carrion biofilm is a mixture of microbes, their metabolites, and compounds released into the matrix directly by beetles or through carrion digestion (24, 26). Microbes, e.g.…”

Section: Discussionmentioning

confidence: 99%

“…excretions) (52). They have antimicrobial effects (37) and, similarly to other carrion beetles (24, 26, 36, 42, 43), probably contain mutualistic microbes. Exudates may however also contain abiotic vectors of heat-generating processes, e.g.…”

Section: Discussionmentioning

confidence: 99%

“…Heat produced in the biofilm may be an external and social mechanism of immune response to entomopathogenic microbes (55–58). Recent studies of Nicrophorus beetles highlighted the importance of beetle-microbe interactions, by indicating that smearing carrion with beetle exudates may simply suppress their microbial competitors (24, 26, 28, 29, 31). Similarly, anal exudates of Necrodes surinamensis were found to have a negative effect on bacterial survival (37).…”

Section: Discussionmentioning

confidence: 99%

“…Carrion beetles, in particular burying beetles (Silphidae: Nicrophorus ), create a biofilm-like matrix on cadavers by applying to its surface anal and oral exudates (24). In case of Nicrophorus the behavior was hypothesized to moisturize carrion (25), facilitate digestion (25–27), suppress microbial competitors (24, 28–31), deter insect competitors by reducing carrion-originating attractants (25, 32, 33), support larval aggregation (25) or development (28) or seed mutualistic microbes and transmit them to offspring (26, 34–36). Exudates of several adult or larval silphid beetles were found to contain antimicrobial compounds (37–41).…”

mentioning

confidence: 99%

“…Moreover, some supposedly mutualistic microbes (e.g. Yarrowia yeasts) were abundantly identified in carrion beetle guts and carrion biofilm (24, 26, 36, 42, 43). Therefore, the biofilm-like matrix on carrion may be viewed as a result of carrion manipulation by beetles.…”

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Heat production in a feeding matrix formed on carrion by communally breeding beetles

Matuszewski

Mądra‐Bielewicz

2019

Preprint

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14Insects regulate their body temperature mostly behaviorally, by changing posture or 15 microhabitat. These strategies may be ineffective in some habitats, for example on carrion. 16 Carrion beetles create a biofilm-like matrix by applying to cadaver surface anal or oral 17 exudates. We tested the hypothesis that biofilm formed by communally breeding Necrodes 18 littoralis L. beetles (Silphidae) produces heat, that enhances beetle fitness. We demonstrated 19 that heat produced in the biofilm is larger than in meat decomposing without insects. Beetles 20 regularly warmed up in the biofilm. Moreover, we provide evidence that biofilm formation by 21 adult beetles has deferred thermal effects for larval microhabitat. We found an increase in heat 22 production of a biofilm and a decrease in development time and mortality of larvae, after 23 adult beetles applied their exudates on meat. Behavioral strategy revealed here for N. littoralis 24 is basically a new form of thermoregulation and parental care in insects. 25 26 Keywords 27 Insect thermoregulation; Animal behavior; Parental care; Carrion ecology; Insect-microbe 28 interactions; Resource competition 29 30 31Temperature is a key component of animal environment. Insects usually use external 32 heat to regulate their body temperature (1, 2). By changing body orientation or selecting 33 microhabitat with specific thermal characteristics, insects may maintain their body 34 temperature within thermal optima (3, 4). These mechanisms may be ineffective at certain 35 developmental stages (e.g. larvae) and in some microhabitats (e.g. carrion or dung), indicating 36 that other thermal options may be important for some insect ectotherms. 37Carrion is an example of a "bonanza" resource, i.e. very rich but at the same time 38 scattered and ephemeral (5). There is severe competition between microbes, insects, and 39 vertebrates over carrion resources (6)(7)(8)(9)(10)(11)(12). Insects, e.g. blow flies (Calliphoridae) or carrion 40 beetles (Silphidae) use carrion for breeding and their larvae are main carrion reducers in 41 terrestrial environments (11, 13, 14). Necrophagous larvae usually feed in aggregations (15). 42Larval aggregates on carrion may have much higher inner temperature than ambient air (by 43 10-30°C), an effect originally discovered in aggregations of larval blow flies (4, 16-20). Heat 44 in these aggregates was hypothesized to derive from microbial activity (21, 22), larval 45 exothermic digestive processes (19) or larval frenetic movements (20, 23). However, the 46 specific mechanisms involved are not known. 47 Carrion beetles, in particular burying beetles (Silphidae: Nicrophorus), create a 48 biofilm-like matrix on cadavers by applying to its surface anal and oral exudates (24). In case 49 of Nicrophorus the behavior was hypothesized to moisturize carrion (25), facilitate digestion 50 (25-27), suppress microbial competitors (24, 28-31), deter insect competitors by reducing 51 carrion-originating attractants (25, 32, 33), support larval aggregation (25) or...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Heat production in a feeding matrix formed on carrion by communally breeding beetles

Matuszewski

Mądra‐Bielewicz

2019

Preprint

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Brood size, food availability, and body size affects male care decisions and offspring performance

Sahm,

Conrad,

Scheu

et al. 2023

Ecology and Evolution

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Wong et al., 2013). Parental care can occur before or after the birth of offspring and includes various behaviors, such as the protection of offspring from predators, the maintenance of a favorable microenvironment and offspring provisioning (Balshine, 2012;Smiseth et al., 2012;Trumbo, 2012) amongst others. Across the animal kingdom, female care is much more widespread than male care (Clutton-Brock, 1991) and even in biparental families, males frequently invest less than females and desert the brood earlier or with a higher probability. The reason for this asymmetry is thought to lie in sex differences in the strength of sexual selection, in the association with the embryo, and in the certainty of parentage (Liker

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Investigating the phylogenetic history of toxin tolerance in mushroom‐feeding Drosophila

Erlenbach,

Haynes,

Fish

et al. 2023

Ecology and Evolution

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Understanding how and when key novel adaptations evolved is a central goal of evolutionary biology. Within the immigrans‐tripunctata radiation of Drosophila, many mushroom‐feeding species are tolerant of host toxins, such as cyclopeptides, that are lethal to nearly all other eukaryotes. In this study, we used phylogenetic and functional approaches to investigate the evolution of cyclopeptide tolerance in the immigrans‐tripunctata radiation of Drosophila. First, we inferred the evolutionary relationships among 48 species in this radiation using 978 single copy orthologs. Our results resolved previous incongruities within species groups across the phylogeny. Second, we expanded on previous studies of toxin tolerance by assaying 16 of these species for tolerance to α‐amanitin and found that six of them could develop on diet with toxin. Finally, we asked how α‐amanitin tolerance might have evolved across the immigrans‐tripunctata radiation, and inferred that toxin tolerance was ancestral in mushroom‐feeding Drosophila and subsequently lost multiple times. Our findings expand our understanding of toxin tolerance across the immigrans‐tripunctata radiation and emphasize the uniqueness of toxin tolerance in this adaptive radiation and the complexity of biochemical adaptations.

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Microbiome-assisted carrion preservation aids larval development in a burying beetle

Cited by 97 publications

References 73 publications

Heat production in a feeding matrix formed on carrion by communally breeding beetles

Heat production in a feeding matrix formed on carrion by communally breeding beetles

Brood size, food availability, and body size affects male care decisions and offspring performance

Investigating the phylogenetic history of toxin tolerance in mushroom‐feeding Drosophila

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