The role of indirect genetic effects in the evolution of interacting reproductive behaviors in the burying beetle,
            Nicrophorus vespilloides

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.

Download Full-text

Analysis of direct and indirect genetic effects in fighting sea anemones

Behavioral Ecology ◽

10.1093/beheco/arz217 ◽

2020 ◽

Vol 31 (2) ◽

pp. 540-547

Author(s):

Sarah M Lane ◽

Alastair J Wilson ◽

Mark Briffa

Keyword(s):

Individual Variation ◽

Theoretical Models ◽

Molecular Data ◽

Genetic Effects ◽

Sea Anemones ◽

Heritable Variation ◽

Evolutionarily Stable Strategies ◽

Fighting Behavior ◽

Indirect Genetic Effects

Abstract Theoretical models of animal contests such as the Hawk-Dove game predict that variation in fighting behavior will persist due to mixed evolutionarily stable strategies (ESS) under certain conditions. However, the genetic basis for this variation is poorly understood and a mixed ESS for fighting can be interpreted in more than one way. Specifically, we do not know whether variation in aggression within a population arises from among-individual differences in fixed strategy (determined by an individual’s genotype—direct genetic effects [DGEs]), or from within-individual variation in strategy across contests. Furthermore, as suggested by developments of the original Hawk-Dove model, within-individual variation in strategy may be dependent on the phenotype and thus genotype of the opponent (indirect genetic effects—IGEs). Here we test for the effect of DGEs and IGEs during fights in the beadlet sea anemone Actinia equina. By exploiting the unusual reproductive system of sea anemones, combined with new molecular data, we investigate the role of both additive (DGE + IGE) and non-additive (DGE × IGE) genetic effects on fighting parameters, the latter of which have been hypothesized but never tested for explicitly. We find evidence for heritable variation in fighting ability and that fight duration increases with relatedness. Fighting success is influenced additively by DGEs and IGEs but we found no evidence for non-additive IGEs. These results indicate that variation in fighting behavior is driven by additive indirect genetic effects (DGE + IGE), and support a core assumption of contest theory that strategies are fixed by DGEs.

Download Full-text

Fitness effects and transmission of phoretic nematodes of the burying beetle, Nicrophorus vespilloides

10.1101/193714 ◽

2017 ◽

Author(s):

Yin Wang ◽

Daniel E. Rozen

Keyword(s):

Brood Size ◽

Larval Survival ◽

List Type ◽

Burying Beetle ◽

Negative Effects ◽

Fitness Effects ◽

Nicrophorus Vespilloides ◽

Males And Females ◽

Efficient Mechanisms

AbstractNicrophorus vespilloides is a cosmopolitan social beetle that rears its offspring on decomposing carrion. Wild beetles are frequently associated with two types of macrobial symbionts, mites and nematodes.Although these organisms are believed to be phoretic commensals that harmlessly use beetles as a means of transfer between carcasses, the role of these symbionts on N. vespilloides fitness is poorly understood. Here we show that nematodes have significant negative effects on beetle fitness across a range of worm densities and also quantify the density-dependent transmission of worms between mating individuals and from parents to offspring.Using field-caught beetles, we provide the first report of a new nematode symbiont in N. vespilloides, most closely related to Rhabditoides regina, and show that worm densities are highly variable across individuals isolated from nature but do not differ between males and females. Next, by inoculating mating females with increasing densities of nematodes, we show that worm infections significantly reduce brood size, larval survival and larval mass, and also eliminate the trade-off between brood size and larval mass. Finally, we show that nematodes are efficiently transmitted between mating individuals and from mothers to larvae, directly and indirectly via the carcass, and that worms persist through pupation.These results show that the phoretic nematode R. regina can be highly parasitic to burying beetles but can nevertheless persist because of efficient mechanisms of intersexual and intergenerational transmission.Phoretic species are exceptionally common and may cause significant harm to their hosts, even though they rely on these larger species for transmission to new resources. However, this harm may be inevitable and unavoidable if transmission of phoretic symbionts requires nematode proliferation. It will be important to determine the generality of our result for other phoretic associates of animals.

Download Full-text

An evolutionary switch from sibling rivalry to sibling cooperation, caused by a sustained loss of parental care

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1911677117 ◽

2020 ◽

Vol 117 (5) ◽

pp. 2544-2550 ◽

Cited By ~ 1

Author(s):

Darren Rebar ◽

Nathan W. Bailey ◽

Benjamin J. M. Jarrett ◽

Rebecca M. Kilner

Keyword(s):

Parental Care ◽

Genetic Effects ◽

Sibling Rivalry ◽

Competitive Behavior ◽

Social Environments ◽

Fitness Costs ◽

Burying Beetle ◽

Evolutionary Mechanisms ◽

Levels Of Care ◽

Indirect Genetic Effects

Sibling rivalry is commonplace within animal families, yet offspring can also work together to promote each other’s fitness. Here we show that the extent of parental care can determine whether siblings evolve to compete or to cooperate. Our experiments focus on the burying beetle Nicrophorus vespilloides, which naturally provides variable levels of care to its larvae. We evolved replicate populations of burying beetles under two different regimes of parental care: Some populations were allowed to supply posthatching care to their young (Full Care), while others were not (No Care). After 22 generations of experimental evolution, we found that No Care larvae had evolved to be more cooperative, whereas Full Care larvae were more competitive. Greater levels of cooperation among larvae compensated for the fitness costs caused by parental absence, whereas parental care fully compensated for the fitness costs of sibling rivalry. We dissected the evolutionary mechanisms underlying these responses by measuring indirect genetic effects (IGEs) that occur when different sibling social environments induce the expression of more cooperative (or more competitive) behavior in focal larvae. We found that indirect genetic effects create a tipping point in the evolution of larval social behavior. Once the majority of offspring in a brood start to express cooperative (or competitive) behavior, they induce greater levels of cooperation (or competition) in their siblings. The resulting positive feedback loops rapidly lock larvae into evolving greater levels of cooperation in the absence of parental care and greater levels of rivalry when parents provide care.

Download Full-text

The role of neuropeptide F in a transition to parental care

Biology Letters ◽

10.1098/rsbl.2016.0158 ◽

2016 ◽

Vol 12 (4) ◽

pp. 20160158 ◽

Cited By ~ 27

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.

Download Full-text

Antimicrobial strategies in burying beetles breeding on carrion

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0805403105 ◽

2008 ◽

Vol 105 (46) ◽

pp. 17890-17895 ◽

Cited By ~ 142

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.

Download Full-text