Quantitative Genetics of Growth and Development Time in the Burying Beetle Nicrophorus Pustulatus in the Presence and Absence of Post-Hatching Parental Care

Abstract

Despite a growing interest in the evolutionary aspects of maternal effects, few studies have examined the genetic consequences of maternal effects associated with parental care. To begin to provide data on nonlaboratory or nondomestic animals, we compared the effect of presence and absence of parental care on phenotype expression of larval mass and development time at different life-history stages in the burying beetle Nicrophorus pustulatus. This beetle has facultative care; parents can feed their larvae through regurgitation of digested carrion or offspring can feed by themselves from previously prepared carrion. To investigate larval responses to these two levels of care, including estimates of additive genetic effects, maternal effects, and genotype-by-environment interactions, we used a half-sibling split-family breeding experiment-raising half of the offspring of a family in the presence of their mother and the other half without their mother present. Larvae reared with their mother present were on average heavier and developed faster, although some of the differences in development decreased or were eliminated by the adult stage. These results suggest that presence or absence of post-hatching maternal care plays an important role in phenotype expression early in life, whereas later the phenotype of the offspring is determined mainly by the genotype and/or unshared environmental effects. Our study also permitted us to examine the differences in genetic effects between the two care environments. Heritabilities, maternal/common environment effect, and most genetic correlations did not differ between the care treatments. Genetic analyses revealed substantial additive genetic effects for development time but small effects for measures of body mass. Maternal plus common environment effects were high for measures of mass but low for development time, suggesting that indirect genetic effects of maternal and/or common environment are less important for the evolution of development time than for mass. Estimates of genetic correlations revealed a trade-off between the duration of the two development stages after the offspring left the carrion. There was also a negative genetic correlation between the time spent on carrion and the mass at 72 h, when mothers usually stop feeding. The analysis of genotype-by-environment interactions indicates substantial variation among maternal families in response to care. Presence or absence of parental care may therefore contribute to the additive genetic variance through its interaction with the maternal component of the additive genetic variance. The presence of this interaction further suggests that parents may vary in care strategies, with some parents dispersing after preparation of the carrion and some parents staying with the larvae. This interaction may help maintain genetic variation in growth, development time, and parental care behavior. Additional work is needed, however, to quantify indirect genetic effects and genetic variation in parental care behavior itself.

Evolutionary importance of parental care performance, food resources, and direct and indirect genetic effects in a burying beetle

“…Adult beetles are active from March to October and reproduction takes place in spring (Anderson & Peck, 1985; Peck & Kaulbars, 1987). Although the reproductive biology of N. pustulatus in the field is not well known, preliminary field data (C. M. Rauter, unpublished data) and breeding experiments in the laboratory (Robertson, 1992; Trumbo, 1992; Rauter & Moore, 2002) indicate that N. pustulatus behaves in the same manner as other burying beetles (reviews by Eggert & Müller, 1997; Scott, 1998). Provided with a dead mouse, N. pustulatus bury the body, remove the fur, work the carrion into a compact ball, and create and maintain a burial chamber.…”

“…A random half (six larvae) of each family was added to the mouse with their genetic mother and the other half (six larvae) was added to the mouse with the foster mother. To control for effects of brood size (Bartlett, 1987; Wilson & Knollenberg, 1987; Bartlett & Ashworth, 1988; Scott & Traniello, 1990), we standardized the number of larvae placed onto a mouse to 12 larvae which is slightly less than the average brood size of 15 larvae for the size of carrion used in the experiment (Rauter & Moore, 2002). Seventy‐two hours after placing the larvae onto the mouse, we weighed all larvae on a mouse to the nearest 0.1 mg. To avoid desertion of the carrion by the female, we removed only six larvae at a time.…”

“…Although the bias arising from this assumption is likely to be small for morphological traits such as body weight, for life history traits such as development time dominance effects can be substantial (Crnokrak & Roff, 1995). Estimates of direct genetic effects on these traits from a previous half‐sib study (Rauter & Moore, 2002) allows us to evaluate the seriousness of this potential bias. Our design also requires that we assume that there are no indirect environmental effects and violations of this assumption would lead to biased estimates of indirect genetic variance.…”

“…Parents with high energetic investment in parental care influence offspring mass positively (Moreno et al ., 1997; Burness et al ., 2001). Provisioning offspring with an energy‐rich and/or a high quality diet improves growth rate of offspring and reduces duration of developmental phases critical for offspring survival (Watanuki, 1992; Johnston, 1993; Meyer et al ., 1994; Rogowitz & McClure, 1995; Rogowitz, 1996; Oksanen et al ., 1999; Hunt & Simmons, 2000; Kunz & Ekman, 2000; Rauter & Moore, 2002). Variation in parental care can therefore result in variation in offspring traits.…”

Interplay between age‐based competitive asymmetries within the brood and direct competition between inbred and outbred offspring in a burying beetle

“…We randomized which hind leg we snipped for seniors and juniors across different broods. Given that adult legs develop from imaginal discs, snipping the legs at the offspring stage has no effect on offspring and adult fitness (Rauter & Moore, ; Smiseth et al., 2007b). Once larvae dispersed from the carcass, we counted the number of seniors and juniors in the brood and weighed seniors and juniors separately (Smiseth & Morgan, ).…”