Michelle Pellissier Scott. American Scientist. Volume 84, Issue 4. Jul/Aug 1996.
When a young chipmunk dies in the woods, a wide variety of organisms-from mammalian scavengers to insects, fungi and microbes compete for this sudden food bonanza. In New England, burying beetles rank as one of the most successful competitors. A chipmunk is a relatively large carcass for these 1.5 centimeter-long insects, and such a food source may be discovered and buried by various combinations of adult burying beetles. As they bury the carcass, they shave it and roll it into a ball, readying it to become food for a single large brood of young, or grubs. Once finished, some of the adults may remain in the brood chamber to tend to the carcass and to feed and defend the larvae until their development is complete.
Among biologists, such an example of apparent cooperation excites special interest, because this behavior appears at first glance to oppose an individual beetle’s best interest. For instance, it seems that a dominant beetle could monopolize a carcass, thereby leaving more offspring of its own, rather than sharing it with another beetle of the same sex. Likewise, a subordinate beetle could look for its own carcass, rather than devote valuable time to helping to rear offspring, most of which are not hers. Societies in which individuals undertake cooperative activities, such as communal breeding, usually also include conflict. Individuals are selected to cooperate only when they gain more than they lose from participating. The balance between cooperation and conflict-between feeding or killing the offspring of another-is a delicate one, and it depends on many factors, including the relatedness of the participants, the alternative options open to each, the relative efficiency of cooperation and the ease with which one individual can dominate others.
Reproductive cooperation and conflict lie at the heart of the evolution of sociality. Communal breeding, in which adults share a nest or a mate and may provide care to another’s young, has been identified as one path leading to complex social systems in both insects and vertebrates. Communal breeding exists in birds, some canids, social insects and only rarely in other groups of animals. Often the participants are related, which gives them some indirect benefit from helping to rear the offspring of a relative.
I have studied the ecology and evolution of reproductive behavior of burying beetles in southern New Hampshire since 1984. They are very informative animals to study, because they are abundant and easy to rear in the laboratory, and because possible causal factors for the evolution of their cooperation can be manipulated experimentally
Behavior and Ecology
Southern New Hampshire hosts four species of burying beetles. Although they partition their habitat temporally by reproducing at somewhat different times during the summer, they overlap in the size of carcass that they are able to bury. The smaller species may rear a few larvae on very small carrion, such as a mouse, which is not buried by a larger species. The medium-size Nicrophorus tomentosus shows the greatest readiness to breed communally. Cooperating groups of N. tomentosus can sometimes bury and prepare larger carcasses that would be difficult for a single pair.
Burying beetles possess highly sensitive chemical receptors in their antennae, which allow them quickly to discover small vertebrate carcasses. Usually a single male and female prepare and bury a carcass. If more than one beetle of the same sex discovers a carcass, they compete fiercely, and usually the larger beetle wins; losers are driven off to nearby vegetation. However, larger carcasses, such as a vole or turkey chick, may be buried by a group of males and females. Arriving beetles first assess the suitability and size of the carcass by walking around its circumference and tasting and lifting it. They may move it to a better spot for burial.
Although beetles can get the carcass out of sight in a few hours, it takes several days to fully bury and prepare a carcass. Females start to lay eggs in the soil nearby 18 to 24 hours after they begin work. These eggs hatch three days later, and the larvae make their way to the top of the carcass, where their parents have cut a hole in its skin. Parents facilitate larval feeding with their proteolytic oral secretions and through direct regurgitation. They also keep the inside and outside of the carcass clean of fungi. Larvae grow very quickly and complete development in seven to nine days, at which time the carcass is generally completely consumed. The duration of maternal and paternal care varies among species, and females usually remain longer than males.
The readiness to breed communally depends, at least in part, on the size of a carcass. No species of burying beetle breeds communally on a small carcass, such as a white-footed mouse. In N. tomentosus, greater carcass size leads to an increased rate of communal breeding: 47 percent on medium (about 45 grams) carcasses, such as a voles, and 75 percent on large (about 70 grams) carcasses, such as juvenile chipmunks. Communal breeding may be more common on larger than on smaller carcasses because the size of the carcass largely determines the number of larvae that can be raised, and females are somewhat limited in the number of eggs that they can lay that will hatch more or less synchronously. Although a female can fully utilize a small carcass by herself, a larger carcass can support many more young than she can produce, and it would also be more difficult for her alone to prepare. Thus a female probably loses less in sharing a large carcass with another female, and both females gain additional assistance.
Although more than one male frequently remains after eggs are laid, females are more likely than males to bury a carcass together. The female that remains in the brood chamber the longest is usually one of the largest. Secondary females may remain after eggs hatch, but secondary males often leave soon after eggs are laid. Rarely do more than a few adults remain in the burial chamber after the larvae appear. Females may be present simultaneously in the burial chamber before eggs hatch, and they do not show any behavioral signs of competition, but observations on brood chambers after larvae are present indicate that two females are seldom present simultaneously to feed and care for larvae. Cooperation, especially in the early stages, may make it possible to raise a larger brood in total, but it is expected to be in the best interests of each female to monopolize reproduction as much as possible.
To understand the origins of different reproductive strategies in these beetles, I had to assess the relative success of each alternative. The first step in that process was identifying which female in a communal nest was the mother of each young beetle. To determine that, Scott Williams of Boston University and I used molecular techniques to match parents with their offspring. In laboratory broods with only two males and two females present, which simplified the task, we found that 70 percent of the females shared a carcass and reared a mixed brood. Likewise, 70 percent of the males also shared reproduction each male inseminated one or both females. The division of maternity of these mixed broods was surprisingly varied, ranging from equitable (nearly 50/50) to extremely inequitable. In the 10 experimental broods, the larger of the two females invariably produced more offspring and remained with the brood longer. The larger male sired more young in 9 of 10 cases, and the male with more young always remained longer.
Why Breed Communally?
Resident beetles must defend their carcass against competitors, especially flies and other burying beetles. Flies have access to a carcass before it is discovered by beetles. And other burying beetles can discover a carcass (even after it has been buried four to five centimeters under ground), evict the residents, kill their brood and produce their own young. So it pays to protect a carcass.
One might expect that smaller beetles would be more likely to cooperate in larger groups as a means of protecting a carcass from other beetles. For instance, does the smaller N. tomentosus breed communally to defend a carcass against the larger burying beetle, N. orbicollis, which also breeds in late summer? Despite the appeal of this idea, my experiments showed that two N. tomentosus can protect a carcass nearly as well as four of them can. For example, a foursome of N. tomentosus can fend off a female N. orbicollis, but a male N. orbicollis often defeats two or four N. tomentosus residents. When proves crucial in the early stages of preparing and ridding a carcass of fly competitors, a dominant female is especially tolerant at that time of both additional males and females in her burial chamber. That time also serves as the critical period for reproductive competition, when males compete to inseminate females, and females deposit their complement of eggs in the nearby soil.
Skewed Reproduction
Despite the potential benefits of communal breeding, a dominant female must still do what she can to limit the number of offspring of other females and to enhance the survival of her offspring. How reproduction is partitioned among adults has recently come to be considered a key characteristic for describing animal societies. Cooperative breeding in birds and mammals and eusociality in complex insect societies form a continuum in which the distribution of lifetime reproductive success among group members provides an important descriptor. Along that continuum, reproduction may be shared equitably, or it may be skewed in favor of some and at the expense of others.
These communally breeding burying beetles share many characteristics with “primitively” social insects, including paper wasps, which form relatively small groups and found colonies with a single female or with a few females that may or may not be related. These insects may establish reproductive dominance through a number of mechanisms, including producing more eggs and then protecting them. Competitors can also be excluded from egg-laying sites, and they can be prevented from engaging in the behavior that promotes egg laying. Social insects with large and complex societies, such as honey bees, are more likely to achieve and maintain reproductive dominance through pheromonal and behavioral suppression of ovarian development.
In order to get a large sample of broods from which to measure the partitioning of reproduction and to investigate how a dominant female might skew reproduction in her favor, I fed one of the female burying beetles in each brood chamber a colored dye that passed quickly to her eggs. When I dug up the brood chamber and surrounding soil and located the eggs, I was able to estimate the number of offspring from each of two females.
Four days after the carcass was buried, just before eggs were expected to hatch, the distribution of eggs laid by two females on a medium carcass was equitable, or at least not statistically different from random, in 42 percent of the broods. The rest of the broods, however, displayed either significant skew or complete monopoly, usually by the larger female. (On large carcasses, reproduction was almost never statistically different from equitable.) Nonetheless, the total number of eggs in these shared broods was significantly less than the sum expected from single females, suggesting that females either suppressed each other’s rate of egg laying or that they destroyed each other’s eggs.
When females are searching for carcasses, their mature ovaries contain partially developed eggs. After locating a carcass, a female’s behavior of assessment and burial cause her eggs to rapidly finish development. Although the dominant female does not prevent the subordinate’s access to the carcass to slow egg development, cooperative burial does significantly stimulate ovarian development for the dominant beetle and suppresses it for the subordinate one. These physiological effects may be mediated hormonally through the behavior of the dominant and subordinate females. The difference in ovarian development, however, is short lived, and both females lay eggs within 24 hours.
Over the next two days, the total number of eggs present in the soil decreases dramatically. Apparently, marauding females can recognize kin and destroy the eggs of competitors. Both the larger and smaller female destroy each other’s eggs in experimental broods, but the larger usually protects her eggs significantly better, even while destroying the smaller beetle’s eggs. When eggs laid by two communally breeding females were identified and counted two days after the dye feeding, the reproductive skew resembled that seen when both females were still present on the fourth day, just before eggs hatched. When the larger, and presumably dominant, female was removed on the second day, the smaller female significantly skewed the brood in her favor by the fourth day This strongly suggests that females can recognize and destroy another beetle’s eggs, and that egg destruction is the most important mechanism for skewing reproduction. Once eggs hatch, adults apparently cannot recognize kin in order to differentially kill unrelated larvae. In fact, adults feed larvae indiscriminately
Shaping the Skew
Several factors may be important in determining whether reproduction is shared equitably or skewed in favor of a dominant beetle. In many animal societies, one individual may help to rear kin and even forgo reproduction. This seemingly altruistic behavior provides an evolutionary advantage in lifetime fitness through the indirect gain of rearing kin, with whom some genes are shared. Nevertheless, even unrelated communally breeding females should not necessarily exhibit equitable reproduction. The proportion of the brood that a female captures should depend on the probability and relative success of independent breedtested against other N. tomentosus, a pair could defend the brood chamber as well as a foursome. So N. tomentosus does not appear to breed communally simply because of its small size.
It turns out that the most important advantage of communal breeding comes during the first few days after discovering a carcass, when the extra beetles help destroy fly eggs and maggots, which could consume the treasure. Flies pose a particularly troublesome problem for N. tomentosus, which is the only species of burying beetle in New Hampshire that is active during the day. Any carcass that these beetles find has probably also been discovered by flies, thereby reducing its value. A pair of beetles rears fewer young on a medium or large fly-infested carcass than do pairs on clean carcasses or foursomes on fly-infested carcasses.
On average the dominant female benefits most from breeding communally. Parentage analysis on laboratory broods reared on medium carcasses indicates that the dominant female produces 80 percent of the total brood. One might ask, why would a subordinate female-who may be the mother of only 20 percent of the brood-remain and help? Although it may seem like too much work for too little profit, keep in mind that she faces an even less appealing alternative-finding her own carcass and breeding alone. Finding a carcass and breeding probably happens only once or twice in a beetle’s short life.
Flies cause a dominant female to gain more than she loses from breeding communally. A communal brood produced in competition with flies may be 32 percent larger on average, compared with the brood of a dominant female reproducing alone. Some of the fiercest competition with flies is in August, when the other species of burying beetles in New Hampshire lose most of the carcasses that they bury to flies and abandon them. N. tomentosus rarely loses a carcass to flies.
As one might expect, the duration of parental care does not depend on the presence or absence of competition from flies. The threat from flies ends after the first few days, when the fly eggs and maggots have been destroyed. In an experiment that compared when adult beetles left a carcass, only the secondary male (the first to leave) stayed a little longer on fly-infested carcasses than on clean ones. Given that helping and the relative fighting ability of the communally breeding females.
Although I have never been able to measure the probability of finding a carcass and breeding in a natural population, the intense competition over carcasses suggests it is a rare event. I have estimated that an average beetle might breed only once, possibly twice, in its lifetime. So the probability is low that independent breeding can serve as an alternative to joining a communal association. Moreover, the lower this probability is, the more a dominant female can take advantage of a subordinate one.
Relative size correlates strongly with relative fighting ability in burying beetles, making it a good predictor of which female will be dominant. Nevertheless, relative size does not predict whether a subordinate female will get close to half or nearly none of a brood. My laboratory experiments showed that the larger female was reproductively dominant about 83 percent of the time, and was the mother of 68 percent and 59 percent of the brood on medium and large carcasses, respectively But the size ratio between the two females did not predict whether the brood was shared more or less equitably, whether it was strongly skewed or whether one female was excluded completely. Once relative status is established there is probably little chance of reversal. So the subordinate is not expected to fight for a bigger share of the brood, unless the probability that she could win exceeds the probability that she could breed independently.
Although relative size is an important determinant in the establishment of dominance, other factors play a role as well. As mentioned above, the discovery of a carcass and its assessment and preparation cause rapid hormonal changes that trigger speedy egg maturation. These endocrine changes probably produce behavioral effects, too. If a female begins to work on a carcass and is joined in two to three hours by a larger female, the smaller female has a greater chance of being reproductively dominant than if the two had discovered the carcass at the same time. In the wild, then, chance events-such as the order in which beetles discover a carcass-must be factored in with ecological parameters-including carcass availability and the degree of competition from other species-to evaluate the outcome of competition between female burying beetles.
As these results show, the evolution of cooperation among nonrelatives depends on a net gain for each of the participants. A subordinate female burying beetle, for example, joins another as long as she can produce some offspring. Rather than laying eggs and deserting, a subordinate female beetle remains to protect her own eggs and to destroy those of other females. After eggs hatch, the subordinate female continues to feed and guard all larvae indiscriminately, as long as her assistance increases the probability that the brood will survive. A dominant female faces a different choice: She can evict subordinates or allow them to remain and limit their share of the brood to the extent possible. She has the least to lose on a large carcass, because she may not be able to fully utilize it alone, and assistance from other adults increases the number of larvae that can be raised. Nevertheless, only a fine line separates cooperation and conflict, and reproductive competition produces extremely variable results.