scholarly journals The transcriptional basis of quantitative behavioral variation

2017 ◽  
Author(s):  
Kyle M. Benowitz ◽  
Elizabeth C. McKinney ◽  
Christopher B. Cunningham ◽  
Allen J. Moore
Keyword(s):  
Gene Expression ◽  
Parental Care ◽  
Behavioral State ◽  
Rna Seq ◽  
Burying Beetle ◽  
Burying Beetles ◽  
Behavioral Variation ◽  
Provisioning Behavior ◽  
Nicrophorus Vespilloides ◽  
Nicrophorus Orbicollis

AbstractWhat causes individuals to produce quantitatively different phenotypes? While substantial research has focused on the allelic changes that affect phenotype, we know less about how gene expression accompanies variable phenotypes. Here, we investigate the transcriptional basis of variation in parental provisioning using two species of burying beetle, Nicrophorus orbicollis and Nicrophorus vespilloides. Specifically, we used RNA-seq to compare the transcriptomes of parents that provided high amounts of provisioning behavior versus low amounts in males and females of each species. We found that there were no overarching transcriptional patterns that distinguish high from low caring parents, and no informative transcripts that displayed particularly large expression differences in females or males. However, we did find more subtle gene expression changes between high and low provisioning parents that are consistent across sexes as well as between the two species. Furthermore, we show that transcripts previously implicated in transitioning into parental care in N. vespilloides had high variance in the levels of transcription and were unusually likely to display differential expression between high and low provisioning parents. Thus, quantitative behavioral variation appears to reflect many transcriptional differences of small effect. We show that nuanced regulation of the same gene products that are required for the transition of one behavioral state to another are also those influencing variation within a behavioral state.Author SummaryBurying beetles in the genus Nicrophorus breed on vertebrate carcasses and provide advanced parental care to their offspring by regurgitating partially digested flesh. However, all adult beetles do not uniformly express this trait. Some provide a large amount of parenting to their offspring, and some only a little. Here, we investigate the genetic causes of why some Nicrophorus beetles feed their offspring more than others. We demonstrate that this difference is likely caused by many small changes in gene expression, rather than a few genes that have major effects. We also find that some of the same genes that help to turn on parental care behavior in burying beetles also seem to play a role in determining how much care a beetle gives. These results provide new angles on longstanding questions about the complexity of the mechanisms that underlie quantitative variation in populations.

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 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 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 Evolved changes in DNA methylation in response to the sustained loss of parental care in the burying beetle

2021 ◽  
Author(s):  
R Mashoodh ◽  
P Sarkies ◽  
J Westoby ◽  
RM Kilner
Keyword(s):  
Gene Expression ◽  
Dna Methylation ◽  
Parental Care ◽  
Experimental Evolution ◽  
Burying Beetle ◽  
Direct Response ◽  
Gene Body Methylation ◽  
Development Environment ◽  
Nicrophorus Vespilloides ◽  
Plastic Changes

AbstractLevels of parental care critically influence the development environment with the capacity to impact the growth, survival, physiology, and behaviour of offspring. Plastic changes in DNA methylation have been hypothesised to modulate gene expression responses to parental environments. Moreover, these effects can be inherited and so may affect the process of adaptive evolution. In this study, using experimental evolution, we investigated how plastic changes in DNA methylation induced by the loss of parental care have evolved in a biparental insect (Nicrophorus vespilloides) using experimental evolution. We show that removal of care in a single generation is associated with changes in gene expression in stress-related pathways in 1st instar larvae. However, in larvae that have adapted to the loss of parental care after being deprived of care for 30 generations, gene expression is shifted from stress-related gene expression towards growth and brain development pathways. We found that changes in gene body methylation arose both as a direct response to the loss of parental care and stochastically as populations diverged. Overall, our results suggest that a complex interplay between transcription and DNA methylation shapes the molecular adaptation to environmental change.

scholarly journals The role of neuropeptide F in a transition to parental care

2016 ◽  
Vol 12 (4) ◽  
pp. 20160158 ◽  
Author(s):  
Christopher B. Cunningham ◽  
Kathryn VanDenHeuvel ◽  
Daven B. Khana ◽  
Elizabeth C. McKinney ◽  
Allen J. Moore
Keyword(s):  
Gene Expression ◽  
Parental Care ◽  
Feeding Behaviour ◽  
Genetic Influences ◽  
Burying Beetle ◽  
Nicrophorus Vespilloides ◽  
Genetic Mechanisms ◽  
Neuropeptide F ◽  
Active Care

The genetics of complex social behaviour can be dissected by examining the genetic influences of component pathways, which can be predicted based on expected evolutionary precursors. Here, we examine how gene expression in a pathway that influences the motivation to eat is altered during parental care that involves direct feeding of larvae. We examine the expression of neuropeptide F , and its receptor, in the burying beetle Nicrophorus vespilloides , which feeds pre-digested carrion to its begging larvae. We found that the npf receptor was greatly reduced during active care. Our research provides evidence that feeding behaviour was a likely target during the evolution of parental care in N. vespilloides . Moreover, dissecting complex behaviours into ethologically distinct sub-behaviours is a productive way to begin to target the genetic mechanisms involved in the evolution of complex behaviours.

scholarly journals Antimicrobial strategies in burying beetles breeding on carrion

2008 ◽  
Vol 105 (46) ◽  
pp. 17890-17895 ◽  
Author(s):  
D. E. Rozen ◽  
D. J. P. Engelmoer ◽  
P. T. Smiseth
Keyword(s):  
Parental Care ◽  
Detrimental Effect ◽  
Larval Growth ◽  
Burying Beetle ◽  
Negative Effects ◽  
Burying Beetles ◽  
Microbial Competition ◽  
Nicrophorus Vespilloides ◽  
Ephemeral Resources

Rich and ephemeral resources, such as carrion, are a source of intense interspecific competition among animal scavengers and microbial decomposers. Janzen [Janzen DH (1977) Am Nat 111:691–713] hypothesized that microbes should be selected to defend such resources by rendering them unpalatable or toxic to animals, and that animals should evolve counterstrategies of avoidance or detoxification. Despite the ubiquity of animal-microbe competition, there are few tests of Janzen's hypothesis, in particular with respect to antimicrobial strategies in animals. Here, we use the burying beetle Nicrophorus vespilloides, a species that obligately breeds on carcasses of small vertebrates, to investigate the role of parental care and avoidance as antimicrobial strategies. We manipulated competition between beetle larvae and microbes by providing beetles with either fresh carcasses or old ones that had reached advanced putrefaction. We found evidence for a strong detrimental effect of microbial competition on beetle reproductive success and larval growth. We also found that parental care can largely compensate for these negative effects, and that when given a choice between old and fresh carcasses, parents tended to choose to rear their broods on the latter. We conclude that parental care and carcass avoidance can function as antimicrobial strategies in this species. Our findings extend the range of behavioral counterstrategies used by animals during competition with microbes, and generalize the work of Janzen to include competition between microbes and insects that rely on carrion as an obligate resource for breeding and not just as an opportunistic meal.

scholarly journals Transcriptomes of parents identify parenting strategies and sexual conflict in a subsocial beetle

2015 ◽  
Vol 6 (1) ◽  
Author(s):  
Darren J. Parker ◽  
Christopher B. Cunningham ◽  
Craig A. Walling ◽  
Clare E. Stamper ◽  
Megan L. Head ◽  
...  
Keyword(s):  
Gene Expression ◽  
Parental Care ◽  
Social Organization ◽  
Sexual Conflict ◽  
Feeding Behaviour ◽  
Burying Beetle ◽  
Parenting Strategies ◽  
The Family ◽  
Nicrophorus Vespilloides ◽  
Female Behaviour

Abstract Parenting in the burying beetle Nicrophorus vespilloides is complex and, unusually, the sex and number of parents that can be present is flexible. Such flexibility is expected to involve specialized behaviour by the two sexes under biparental conditions. Here, we show that offspring fare equally well regardless of the sex or number of parents present. Comparing transcriptomes, we find a largely overlapping set of differentially expressed genes in both uniparental and biparental females and in uniparental males including vitellogenin, associated with reproduction, and takeout, influencing sex-specific mating and feeding behaviour. Gene expression in biparental males is similar to that in non-caring states. Thus, being ‘biparental’ in N. vespilloides describes the family social organization rather than the number of directly parenting individuals. There was no specialization; instead, in biparental families, direct male parental care appears to be limited with female behaviour unchanged. This should lead to strong sexual conflict.

scholarly journals Predictable gene expression related to behavioral variation in parenting

2018 ◽  
Vol 30 (2) ◽  
pp. 402-407 ◽  
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.

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).  

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