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 ◽  
...  

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.

2016 ◽  
Vol 12 (4) ◽  
pp. 20160158 ◽  
Author(s):  
Christopher B. Cunningham ◽  
Kathryn VanDenHeuvel ◽  
Daven B. Khana ◽  
Elizabeth C. McKinney ◽  
Allen J. Moore

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.


2021 ◽  
Author(s):  
R Mashoodh ◽  
P Sarkies ◽  
J Westoby ◽  
RM Kilner

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.


2017 ◽  
Author(s):  
Kyle M. Benowitz ◽  
Elizabeth C. McKinney ◽  
Christopher B. Cunningham ◽  
Allen J. Moore

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.


2021 ◽  
Vol 118 (48) ◽  
pp. e2102450118
Author(s):  
Ana Duarte ◽  
Darren Rebar ◽  
Allysa C. Hallett ◽  
Benjamin J. M. Jarrett ◽  
Rebecca M. Kilner

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.


2018 ◽  
Vol 30 (2) ◽  
pp. 402-407 ◽  
Author(s):  
Kyle M Benowitz ◽  
Elizabeth C McKinney ◽  
Christopher B Cunningham ◽  
Allen J Moore

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.


1970 ◽  
Vol 21 (1) ◽  
pp. 47-54
Author(s):  
Sharmin Musa

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).  


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3278 ◽  
Author(s):  
Sonia Pascoal ◽  
Rebecca M. Kilner

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.


2018 ◽  
Vol 285 (1885) ◽  
pp. 20181452 ◽  
Author(s):  
Benjamin J. M. Jarrett ◽  
Darren Rebar ◽  
Hannah B. Haynes ◽  
Miranda R. Leaf ◽  
Chay Halliwell ◽  
...  

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.


2019 ◽  
Vol 30 (5) ◽  
pp. 1443-1450 ◽  
Author(s):  
Richard Grew ◽  
Tom Ratz ◽  
Jon Richardson ◽  
Per T Smiseth

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.


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