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 ◽  
...  

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.

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.


2015 ◽  
Author(s):  
William JP Palmer ◽  
Ana Duarte ◽  
Matthew Schrader ◽  
Jonathan P Day ◽  
Rebecca Kilner ◽  
...  

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.


2008 ◽  
Vol 105 (46) ◽  
pp. 17890-17895 ◽  
Author(s):  
D. E. Rozen ◽  
D. J. P. Engelmoer ◽  
P. T. Smiseth

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.


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.


2018 ◽  
Author(s):  
D. Rebar ◽  
H. C. Leggett ◽  
S.M.L. Aspinall ◽  
A. Duarte ◽  
R.M. Kilner

ABSTRACTAnimals are now known to be intimately associated with microbial communities, some of which enhance animal fitness. Yet relatively little is known about how these beneficial associations initially arose. We investigated this problem with an experiment on burying beetles, Nicrophorus vespilloides, which breed on the body of a small dead vertebrate. We found that burying beetles breeding on germ-free mice produced smaller larvae, with lower fitness, than those breeding on conventional germ-laden mice. Thus, burying beetles gain benefits from the microbial community associated with their carrion breeding resource, because they lose fitness when this community is removed experimentally. Our experiment suggests that a symbiosis between an animal and a microbial community might begin as an adaptation to the microbial ecosystem in which the animal lives, even when these microbes exist outside the animal, are transiently associated with it at each generation and are not directly transmitted from parents to offspring.


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.


2019 ◽  
Vol 30 (5) ◽  
pp. 1477-1487 ◽  
Author(s):  
Jon Richardson ◽  
Jennifer Ross ◽  
Per T Smiseth

Abstract Individuals vary with respect to their nutritional state and such variation is an important determinant of the amount of resources individuals allocate toward reproductive functions. Currently, we have a relatively poor understanding of the downstream consequences of food deprivation on different traits associated with reproduction. Here, we address this gap by investigating how food deprivation affected different traits across the breeding cycle in the burying beetle, Nicrophorus vespilloides; a species that breeds on carcasses of small vertebrates serving as food for both parents and offspring. We found that food-deprived females took longer to start egg laying than control females, which may allow them more time to feed from the carcass. There was no difference between food-deprived and control females in the number, size, laying pattern, or hatching success of eggs, suggesting that this delay allowed females to compensate for their poor initial state. However, food-deprived females spent less time providing care, suggesting that this compensation was incomplete. Finally, we found no evidence for negative effects of food deprivation on the offspring’s growth or survival, which is surprising given that food-deprived females took longer to initiate egg laying and provided less care to their offspring. Our results highlight that food deprivation can have complex effects on parental and offspring traits, and suggest that females face a trade-off between the benefits of mitigating downstream consequences of nutritional stress and the costs associated with delaying the start of reproduction.


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.


Author(s):  
Tom Ratz ◽  
Katy M Monteith ◽  
Pedro F Vale ◽  
Per T Smiseth

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.


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