scholarly journals Adaptation to a novel family environment involves both apparent and cryptic phenotypic changes

2017 ◽  
Vol 284 (1862) ◽  
pp. 20171295 ◽  
Author(s):  
Matthew Schrader ◽  
Benjamin J. M. Jarrett ◽  
Darren Rebar ◽  
Rebecca M. Kilner

Cryptic evolution occurs when evolutionary change is masked by concurrent environmental change. In most cases, evolutionary changes in the phenotype are masked by changing abiotic factors. However, evolutionary change in one trait might also be masked by evolutionary change in another trait, a phenomenon referred to as evolutionary environmental deterioration. Nevertheless, detecting this second type of cryptic evolution is challenging and there are few compelling examples. Here, we describe a likely case of evolutionary environmental deterioration occurring in experimental burying beetle ( Nicrophorus vespilloides ) populations that are adapting to a novel social environment that lacks post-hatching parental care. We found that populations rapidly adapted to the removal of post-hatching parental care. This adaptation involved clear increases in breeding success and larval density (number of dispersing larvae produced per gram of breeding carcass), which in turn masked a concurrent increase in the mean larval mass across generations. This cryptic increase in larval mass was accomplished through a change in the reaction norm that relates mean larval mass to larval density. Our results suggest that cryptic evolution might be commonplace in animal families, because evolving trophic and social interactions can potentially mask evolutionary change in other traits, like body size.

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.


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.


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.


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.


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 ◽  
Vol 83 (9) ◽  
Author(s):  
Yin Wang ◽  
Daniel E. Rozen

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.


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.


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