Olfactory Choice for Decomposition Stage in the Burying Beetle Nicrophorus vespilloides: Preference or Aversion?

Sensory cues predicting resource quality are drivers of key animal behaviors such as preference or aversion. Despite the abundance of behavioral choice studies across the animal kingdom, relatively few studies have tested whether these decisions are driven by preference for one choice or aversion to another. In the burying beetle Nicrophorus vespilloides, adult pairs exhibit parental care to raise their offspring on a small carrion resource. We tested whether carrion decomposition stage affected brood quantity and quality and found that mating pairs had significantly more offspring on fresher carcasses. To determine whether this observed reproductive benefit correlates with maternal preference behavior, we conducted a series of olfactory trials testing mated female preferences for mouse carcasses of differing decomposition stages. When given the option between fresh and older carcasses, females associated significantly more with fresher, 1-day old carcasses. However, this behavior may be driven by aversion, as females that were given a choice between the 7-day old carcass and a blank control spent significantly more time in the control chamber. We characterized volatile organic compound profiles of both carcass types, highlighting unique compounds that may serve as public information (sensu lato) conveying resource quality information to gravid beetles.

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1812808115 ◽

2018 ◽

Vol 115 (44) ◽

pp. 11274-11279 ◽

Cited By ~ 32

Author(s):

Shantanu P. Shukla ◽

Camila Plata ◽

Michael Reichelt ◽

Sandra Steiger ◽

David G. Heckel ◽

...

Keyword(s):

Microbial Community ◽

Larval Development ◽

Free Amino ◽

Management Strategy ◽

Larval Growth ◽

Burying Beetle ◽

Microbial Succession ◽

Wide Range ◽

Nicrophorus Vespilloides ◽

Carrion Decomposition

The ability to feed on a wide range of diets has enabled insects to diversify and colonize specialized niches. Carrion, for example, is highly susceptible to microbial decomposers, but is kept palatable several days after an animal’s death by carrion-feeding insects. Here we show that the burying beetle Nicrophorus vespilloides preserves carrion by preventing the microbial succession associated with carrion decomposition, thus ensuring a high-quality resource for their developing larvae. Beetle-tended carcasses showed no signs of degradation and hosted a microbial community containing the beetles’ gut microbiota, including the yeast Yarrowia. In contrast, untended carcasses showed visual and olfactory signs of putrefaction, and their microbial community consisted of endogenous and soil-originating microbial decomposers. This regulation of the carcass’ bacterial and fungal community and transcriptomic profile was associated with lower concentrations of putrescine and cadaverine (toxic polyamines associated with carcass putrefaction) and altered levels of proteases, lipases, and free amino acids. Beetle-tended carcasses develop a biofilm-like matrix housing the yeast, which, when experimentally removed, leads to reduced larval growth. Thus, tended carcasses hosted a mutualistic microbial community that promotes optimal larval development, likely through symbiont-mediated extraintestinal digestion and detoxification of carrion nutrients. The adaptive preservation of carrion coordinated by the beetles and their symbionts demonstrates a specialized resource-management strategy through which insects modify their habitats to enhance fitness.

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Experience does not alter alternative mating tactics in the burying beetle Nicrophorus vespilloides

Behavioral Ecology ◽

10.1093/beheco/arn127 ◽

2008 ◽

Vol 20 (1) ◽

pp. 153-159 ◽

Cited By ~ 15

Author(s):

Craig A. Walling ◽

Clare E. Stamper ◽

Claire L. Salisbury ◽

Allen J. Moore

Keyword(s):

Alternative Mating Tactics ◽

Burying Beetle ◽

Mating Tactics ◽

Nicrophorus Vespilloides

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Peer Review #1 of "Development and application of 14 microsatellite markers in the burying beetle Nicrophorus vespilloides reveals population genetic differentiation at local spatial scales (v0.1)"

10.7287/peerj.3278v0.1/reviews/1 ◽

2017 ◽

Keyword(s):

Genetic Differentiation ◽

Microsatellite Markers ◽

Peer Review ◽

Population Genetic ◽

Spatial Scales ◽

Burying Beetle ◽

Population Genetic Differentiation ◽

Nicrophorus Vespilloides

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2102450118 ◽

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.

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Maternal effects alter the severity of inbreeding depression in the offspring

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.1023 ◽

2016 ◽

Vol 283 (1838) ◽

pp. 20161023 ◽

Cited By ~ 18

Author(s):

Natalie Pilakouta ◽

Per T. Smiseth

Keyword(s):

Maternal Effects ◽

Inbreeding Depression ◽

Potential Role ◽

Causal Effect ◽

Natural Populations ◽

Larval Survival ◽

Burying Beetle ◽

Nicrophorus Vespilloides ◽

Selection For

A maternal effect is a causal influence of the maternal phenotype on the offspring phenotype over and above any direct effects of genes. There is abundant evidence that maternal effects can have a major impact on offspring fitness. Yet, no previous study has investigated the potential role of maternal effects in influencing the severity of inbreeding depression in the offspring. Inbreeding depression is a reduction in the fitness of inbred offspring relative to outbred offspring. Here, we tested whether maternal effects due to body size alter the magnitude of inbreeding depression in the burying beetle Nicrophorus vespilloides . We found that inbreeding depression in larval survival was more severe for offspring of large females than offspring of small females. This might be due to differences in how small and large females invest in an inbred brood because of their different prospects for future breeding opportunities. To our knowledge, this is the first evidence for a causal effect of the maternal phenotype on the severity of inbreeding depression in the offspring. In natural populations that are subject to inbreeding, maternal effects may drive variation in inbreeding depression and therefore contribute to variation in the strength and direction of selection for inbreeding avoidance.

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Inbred burying beetles suffer fitness costs from making poor decisions

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.0419 ◽

2018 ◽

Vol 285 (1881) ◽

pp. 20180419 ◽

Cited By ~ 1

Author(s):

Jon Richardson ◽

Pauline Comin ◽

Per T. Smiseth

Keyword(s):

Decision Making ◽

Inbreeding Depression ◽

Resource Availability ◽

Environmental Conditions ◽

Fitness Costs ◽

Individual Decision ◽

Burying Beetle ◽

Individual Decision Making ◽

Fitness Consequences ◽

Nicrophorus Vespilloides

There is growing interest in how environmental conditions, such as resource availability, can modify the severity of inbreeding depression. However, little is known about whether inbreeding depression is also associated with differences in individual decision-making. For example, decisions about how many offspring to produce are often based upon the prevailing environmental conditions, such as resource availability, and getting these decisions wrong may have important fitness consequences for both parents and offspring. We tested for effects of inbreeding on individual decision-making in the burying beetle Nicrophorus vespilloides, which uses the size of a carrion resource to make decisions about number of offspring. Both inbred and outbred females adjusted their initial decisions about number of eggs to lay based on carcass size. However, when we forced individuals to update this initial decision by providing them with a different-sized carcass partway through reproduction, inbred females failed to update their decision about how many larvae to cull. Consequently, inbred females reared too many larvae, resulting in negative fitness consequences in the form of smaller offspring and reduced female post-reproductive condition. Our study provides novel insights into the effects of inbreeding by showing that poor decision-making by inbred individuals can negatively affect fitness.

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Predictable gene expression related to behavioral variation in parenting

Behavioral Ecology ◽

10.1093/beheco/ary179 ◽

2018 ◽

Vol 30 (2) ◽

pp. 402-407 ◽

Cited By ~ 3

Author(s):

Kyle M Benowitz ◽

Elizabeth C McKinney ◽

Christopher B Cunningham ◽

Allen J Moore

Keyword(s):

Gene Expression ◽

A Priori ◽

Behavioral Changes ◽

Biological Functions ◽

Burying Beetle ◽

Behavioral Transitions ◽

Nicrophorus Vespilloides ◽

Differential Gene ◽

The Relationship ◽

Single Phenotype

AbstractDifferential gene expression has been associated with transitions between behavioral states for a wide variety of organisms and behaviors. Heterochrony, genetic toolkits, and predictable pathways underlying behavioral transitions have been hypothesized to explain the relationship between transcription and behavioral changes. Less studied is how variation in transcription is related to variation within a behavior, and if the genes that are associated with this variation are predictable. Here, we adopt an evolutionary systems biology perspective to address 2 hypotheses relating differential expression to changes within and between behavior. We predicted fewer genes will be associated with variation within a behavior than with transitions between states, and the genes underlying variation within a behavior will represent a narrower set of biological functions. We tested for associations with parenting variation within a state with a set of genes known a priori to be differentially expressed (DE) between parenting states in the burying beetle Nicrophorus vespilloides. As predicted, we found that far fewer genes are DE related to variation within parenting. Moreover, these were not randomly distributed among categories or pathways in the gene set we tested and primarily involved genes associated with neurotransmission. We suggest that this means candidate genes will be easier to identify for associations within a behavior, as descriptions of behavioral state may include more than a single phenotype.

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