scholarly journals Gut Microbiota Colonization and Transmission in the Burying Beetle Nicrophorus vespilloides throughout Development

2017 ◽  
Vol 83 (9) ◽  
Author(s):  
Yin Wang ◽  
Daniel E. Rozen
Keyword(s):  
Gut Microbiota ◽  
Parental Care ◽  
Insect Behavior ◽  
Larval Feeding ◽  
Burying Beetle ◽  
Content Type ◽  
Gut Colonization ◽  
Nicrophorus Vespilloides ◽  
Parental Treatment ◽  
Carrion Beetles

ABSTRACT Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization. IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus vespilloides. This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.

scholarly journals Colonization and transmission of the gut microbiota of the burying beetle,Nicrophorus vespolloides, through development

2016 ◽  
Author(s):  
Yin Wang ◽  
Daniel E. Rozen
Keyword(s):  
Gut Microbiota ◽  
Parental Care ◽  
Insect Behavior ◽  
Larval Feeding ◽  
Burying Beetle ◽  
Treatment Groups ◽  
Gut Colonization ◽  
Nicrophorus Vespilloides ◽  
Parental Treatment ◽  
Carrion Beetles

AbstractCarrion beetles in the genusNicrophorusrear their offspring on decomposing carcasses where larvae are exposed to a diverse microbiome of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as Pre-Hatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as Full care). Here we partition the roles of pre- and post-hatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (Full-Care, Pre-Hatch care only, and No Care), we found that larvae receiving Full-Care are predominantly colonized by bacteria resident in the maternal gut, while larvae receiving No Care are colonized exclusively with bacteria from the carcass. More importantly, larvae receiving only Pre-Hatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo a aposymbiotic stage, after which they are recolonized at eclosion with bacteria shed in the moulted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of pre-hatch parental care for symbiont transmission inNicrophorus vespilloides, and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.ImportanceHere we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetleNicrophorus vespilloides.This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses where they are exposed to high-densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation, but are recolonized from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further indicate that strong competitive interactions mediate the bacterial composition ofNicrophoruslarvae, suggesting that the bacterial communities of these insects may be highly coevolved with their host species.

scholarly journals Evolutionary change in the construction of the nursery environment when parents are prevented from caring for their young directly

2021 ◽  
Vol 118 (48) ◽  
pp. e2102450118
Author(s):  
Ana Duarte ◽  
Darren Rebar ◽  
Allysa C. Hallett ◽  
Benjamin J. M. Jarrett ◽  
Rebecca M. Kilner
Keyword(s):  
Parental Care ◽  
Experimental Evolution ◽  
Evolutionary Change ◽  
Direct Care ◽  
Dead Body ◽  
Extended Phenotype ◽  
Burying Beetle ◽  
Burying Beetles ◽  
Nicrophorus Vespilloides ◽  
Cross Fostering

Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations—for reasons that remain unclear.

scholarly journals The Importance Of Pre-Hatching Paternal Care On Offspring Fitness In Burying Beetle, Nicrophorus Vespilloides Herbst.

1970 ◽  
Vol 21 (1) ◽  
pp. 47-54
Author(s):  
Sharmin Musa
Keyword(s):  
Treatment Group ◽  
Parental Care ◽  
Paternal Care ◽  
Male Parent ◽  
Direct Care ◽  
Removal Experiment ◽  
Burying Beetle ◽  
Offspring Fitness ◽  
Nicrophorus Vespilloides ◽  
Positive Effect

A male-removal experiment was performed to determine if the value of male parental care depended on the timing of the help. In the experiment male parent was removed before the carcass was prepared for breeding, after partial carcass preparation, after complete carcass preparation, before direct care for the larvae and males were allowed to disperse naturally after caring for the larvae. It was found that where the male provided complete pre-hatching care or both preand post-hatching care offspring were larger and in better condition. Mass of offspring at eclosion was affected by male removal (F3,1266 = 5.087, p = 0.002) though size of offspring was not affected by the treatment group. Complete prehatching care had a positive effect on development compared to limited care (F3, 1267 = 8.501, p < 0.000) but this effect disappeared if males remained after the larvae hatched. Larval survivorship did not vary among treatments (F3,122 = 0.531, p = 0.662).  

scholarly journals Development and application of 14 microsatellite markers in the burying beetle Nicrophorus vespilloides reveals population genetic differentiation at local spatial scales

PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3278 ◽  
Author(s):  
Sonia Pascoal ◽  
Rebecca M. Kilner
Keyword(s):  
Genetic Differentiation ◽  
Microsatellite Markers ◽  
Parental Care ◽  
Social Evolution ◽  
Spatial Scales ◽  
Burying Beetle ◽  
Genetic Structuring ◽  
Population Genetic Differentiation ◽  
Nicrophorus Vespilloides ◽  
Limited Dispersal

Burying beetles (genus Nicrophorus) are relatively rare among insects in providing sophisticated parental care. Consequently, they have become model species in research analysing social evolution, the evolution of parental care and mating systems. We used the recently published N. vespilloides genome and transcriptome to develop microsatellite markers. Specifically, we developed 14 polymorphic markers with five to 13 alleles per locus and used them to investigate levels of genetic differentiation in four south Cambridgeshire (UK) populations of N. vespilloides, separated by 21 km at most. The markers revealed significant genetic structuring among populations (global FST = 0.023) with all but one of the pairwise comparisons among populations being significant. The single exception was the comparison between the two closest populations, which are approximately 2.5 km apart. In general, the microsatellite markers showed lower observed heterozygosity than expected. We infer that there is limited dispersal between populations and potentially also some inbreeding within them and suggest that this may be due to habitat fragmentation. We discuss these results in the context of recent laboratory experiments on inbreeding and beetle flight.

scholarly journals Adaptive evolution of synchronous egg-hatching in compensation for the loss of parental care

2018 ◽  
Vol 285 (1885) ◽  
pp. 20181452 ◽  
Author(s):  
Benjamin J. M. Jarrett ◽  
Darren Rebar ◽  
Hannah B. Haynes ◽  
Miranda R. Leaf ◽  
Chay Halliwell ◽  
...  
Keyword(s):  
Parental Care ◽  
The Body ◽  
Burying Beetle ◽  
Burying Beetles ◽  
Egg Hatching ◽  
Asynchronous Hatching ◽  
Nicrophorus Vespilloides ◽  
Experimental Populations ◽  
And Control ◽  
Better Than

Interactions among siblings are finely balanced between rivalry and cooperation, but the factors that tip the balance towards cooperation are incompletely understood. Previous observations of insect species suggest that (i) sibling cooperation is more likely when siblings hatch at the same time, and (ii) this is more common when parents provide little to no care. In this paper, we tested these ideas experimentally with the burying beetle, Nicrophorus vespilloides . Burying beetles convert the body of a small dead vertebrate into an edible nest for their larvae, and provision and guard their young after hatching. In our first experiment, we simulated synchronous or asynchronous hatching by adding larvae at different intervals to the carrion-breeding resource. We found that ‘synchronously’ hatched broods survived better than ‘asynchronously’ hatched broods, probably because ‘synchronous hatching’ generated larger teams of larvae, that together worked more effectively to penetrate the carrion nest and feed upon it. In our second experiment, we measured the synchronicity of hatching in experimental populations that had evolved for 22 generations without any post-hatching care, and control populations that had evolved in parallel with post-hatching care. We found that larvae were more likely to hatch earlier, and at the same time as their broodmates, in the experimental populations that evolved without post-hatching care. We suggest that synchronous hatching enables offspring to help each other when parents are not present to provide care. However, we also suggest that greater levels of cooperation among siblings cannot compensate fully for the loss of parental care.

scholarly journals Parental care buffers against effects of ambient temperature on offspring performance in an insect

2019 ◽  
Vol 30 (5) ◽  
pp. 1443-1450 ◽  
Author(s):  
Richard Grew ◽  
Tom Ratz ◽  
Jon Richardson ◽  
Per T Smiseth
Keyword(s):  
Ambient Temperature ◽  
Parental Care ◽  
Female Parent ◽  
Larval Survival ◽  
Climatic Conditions ◽  
Burying Beetle ◽  
Offspring Performance ◽  
Behavioral Mechanism ◽  
Wide Range ◽  
Nicrophorus Vespilloides

AbstractUnderstanding how animals respond to and cope with variation in ambient temperature is an important priority. The reason for this is that ambient temperature is a key component of the physical environment that influences offspring performance in a wide range of ectotherms and endotherms. Here, we investigate whether posthatching parental care provides a behavioral mechanism for buffering against the effects of ambient temperature on offspring in the burying beetle Nicrophorus vespilloides. We used a 3 × 2 factorial design where we manipulated ambient temperature (15, 20, or 25 °C) and parental care (presence or absence of a female parent after hatching). We found that the effect of ambient temperature on offspring performance was conditional upon the presence or absence of a caring female. Fewer larvae survived in the absence than in the presence of a caring female at 15 °C while there was no difference in larval survival at 20 and 25 °C. Our results show that parental care buffers against some of the detrimental effects of variation in ambient temperature on offspring. We suggest that posthatching parental care may buffer against such effects by creating a more benign environment or by boosting offspring resilience toward stressors. Our results have important implications for our understanding of the evolution of parental care because they suggest that the evolution of parental care could allow species to expand their geographical range to colonize areas with harsher climatic conditions than they otherwise would tolerate.

scholarly journals Carry on caring: infected females maintain their parental care despite high mortality

2021 ◽  
Author(s):  
Tom Ratz ◽  
Katy M Monteith ◽  
Pedro F Vale ◽  
Per T Smiseth
Keyword(s):  
Parental Care ◽  
Disease Transmission ◽  
Reproductive Output ◽  
Sickness Behavior ◽  
Immune Gene ◽  
Burying Beetle ◽  
Immune Genes ◽  
Levels Of Care ◽  
Nicrophorus Vespilloides ◽  
High Level

Abstract Parental care is a key component of an organism’s reproductive strategy that is thought to trade-off with allocation toward immunity. Yet, it is unclear how caring parents respond to pathogens: do infected parents reduce care as a sickness behavior or simply from being ill or do they prioritize their offspring by maintaining high levels of care? To address this issue, we investigated the consequences of infection by the pathogen Serratia marcescens on mortality, time spent providing care, reproductive output, and expression of immune genes of female parents in the burying beetle Nicrophorus vespilloides. We compared untreated control females with infected females that were inoculated with live bacteria, immune-challenged females that were inoculated with heat-killed bacteria, and injured females that were injected with buffer. We found that infected and immune-challenged females changed their immune gene expression and that infected females suffered increased mortality. Nevertheless, infected and immune-challenged females maintained their normal level of care and reproductive output. There was thus no evidence that infection led to either a decrease or an increase in parental care or reproductive output. Our results show that parental care, which is generally highly flexible, can remain remarkably robust and consistent despite the elevated mortality caused by infection by pathogens. Overall, these findings suggest that infected females maintain a high level of parental care, a strategy that may ensure that offspring receive the necessary amount of care but that might be detrimental to the parents’ own survival or that may even facilitate disease transmission to offspring.

scholarly journals A gene for social immunity in the burying beetle Nicrophorus vespilloides?

2015 ◽  
Author(s):  
William JP Palmer ◽  
Ana Duarte ◽  
Matthew Schrader ◽  
Jonathan P Day ◽  
Rebecca Kilner ◽  
...  
Keyword(s):  
Immune System ◽  
Parental Care ◽  
Microbial Growth ◽  
Group Living ◽  
Social Immunity ◽  
Burying Beetle ◽  
Burying Beetles ◽  
Nicrophorus Vespilloides ◽  
Living Species ◽  
Six Genes

Some group-living species exhibit social immunity, where the immune system of one individual can protect others in the group from infection. In burying beetles this is part of parental care. Larvae feed on vertebrate carcasses which their parents smear with exudates that inhibit microbial growth. We have sequenced the transcriptome of the burying beetle Nicrophorus vespilloides and identified six genes that encode lysozymes – a type of antimicrobial enzyme that has previously been implicated in social immunity in burying beetles. When females start breeding and producing antimicrobial anal exudates, we found that the expression of one of these genes was increased by ~1000 times to become one of the most abundant transcripts in the transcriptome. We conclude that we have likely identified a gene for social immunity, and that it was recruited during evolution from a previous function in personal immunity.

scholarly journals In Vitro Gut Modeling as a Tool for Adaptive Evolutionary Engineering of Lactiplantibacillus plantarum

mSystems ◽  
2021 ◽  
Vol 6 (2) ◽  
Author(s):  
Julia Isenring ◽  
Annelies Geirnaert ◽  
Alex R. Hall ◽  
Christoph Jans ◽  
Christophe Lacroix ◽  
...  
Keyword(s):  
Gut Microbiota ◽  
Model Organism ◽  
Strain Improvement ◽  
Evolutionary Engineering ◽  
Bacterial Strains ◽  
Content Type ◽  
Colonic Microbiota ◽  
Gut Colonization ◽  
Fermentation Model

ABSTRACT Research and marketing of probiotics demand holistic strain improvement considering both the biotic and abiotic gut environment. Here, we aim to establish the continuous in vitro colonic fermentation model PolyFermS as a tool for adaptive evolutionary engineering. Immobilized fecal microbiota from adult donors were steadily cultivated up to 72 days in PolyFermS reactors, providing a long-term compositional and functional stable ecosystem akin to the donor’s gut. Inoculation of the gut microbiota with immobilized or planktonic Lactiplantibacillus plantarum NZ3400, a derivative of the probiotic model strain WCFS1, led to successful colonization. Whole-genome sequencing of 45 recovered strains revealed mutations in 16 genes involved in signaling, metabolism, transport, and cell surface. Remarkably, mutations in LP_RS14990, LP_RS15205, and intergenic region LP_RS05100<LP_RS05095 were found in recovered strains from different adaptation experiments. Combined addition of the reference strain NZ3400 and each of those mutants to the gut microbiota resulted in increased abundance of the corresponding mutant in PolyFermS microbiota after 10 days, showing the beneficial nature of these mutations. Our data show that the PolyFermS system is a suitable technology to generate adapted mutants for colonization under colonic conditions. Analysis thereof will provide knowledge about factors involved in gut microbiota colonization and persistence. IMPORTANCE Improvement of bacterial strains in regard to specific abiotic environmental factors is broadly used to enhance strain characteristics for processing and product quality. However, there is currently no multidimensional probiotic strain improvement approach for both abiotic and biotic factors of a colon microbiota. The continuous PolyFermS fermentation model allows stable and reproducible continuous cultivation of colonic microbiota and provides conditions akin to the host gut with high control and easy sampling. This study investigated the suitability of PolyFermS for adaptive evolutionary engineering of a probiotic model organism for lactobacilli, Lactiplantibacillus plantarum, to an adult human colonic microbiota. The application of PolyFermS controlled gut microbiota environment led to adaptive evolution of L. plantarum strains for enhanced gut colonization characteristics. This novel tool for strain improvement can be used to reveal relevant factors involved in gut microbiota colonization and develop adapted probiotic strains with improved functionality in the gut.

Sign in / Sign up

Export Citation Format

Share Document