Conflict within species determines the value of a mutualism between species

Abstract

Mutually beneficial interactions between species play a key role in maintaining biodiversity and ecosystem function. Nevertheless, such mutualisms can erode into antagonistic interactions. One explanation is that the fitness costs and benefits of interacting with a partner species vary among individuals. However, it is unclear why such variation exists. Here, we demonstrate that social behavior within species plays an important, though hitherto overlooked, role in determining the relative fitness to be gained from interacting with a second species. By combining laboratory experiments with field observations, we report that conflict within burying beetles Nicrophorus vespilloides influences the fitness that can be gained from interacting with the mite Poecilochirus carabi. Beetles transport these mites to carrion, upon which both species breed. We show that mites help beetles win intraspecific contests for this scarce resource: mites raise beetle body temperature, which enhances beetle competitive prowess. However, mites confer this benefit only upon smaller beetles, which are otherwise condemned by their size to lose contests for carrion. Larger beetles need no assistance to win a carcass and then lose reproductive success when breeding alongside mites. Thus, the extent of mutualism is dependent on an individual's inability to compete successfully and singlehandedly with conspecifics. Mutualisms degrade into antagonism when interactions with a partner species start to yield a net fitness loss, rather than a net fitness gain. This study suggests that interactions with conspecifics determine where this tipping point lies.

Keywords: Conflict; cooperation; fighting; social behavior; social evolution.

Figure 1

The independent effects of mites and temperature on contest outcome. Beetles were evenly matched for body size in all contests. Numbers indicate trials won by beetles.

Figure 2

The effect of mite association on body temperature 2 sec before and 2 sec after each contest. The median, inter‐quartile range, and range of data are shown in the boxplots. Each boxplot shows data from 80 acts of aggression. “Temperature difference” refers to the difference between temperature of the beetle and the temperature of the soil it is on.

Figure 3

The effect of mites on burying beetle body temperature during exercise and subsequent rest. “Temperature difference” refers to the difference between the temperature of the beetle during the experiment and at the start of the respective experiment (see Methods section for more details). This is shown for the different loading treatments across time, during walking by (A) small beetles and (B) large beetles, and during the subsequent resting period for (C) small beetles and (D) large beetles. Inset images show the different loads borne by beetles in the different experimental treatments: (A) weight (C) and 30 mites. n = 17 for both small and large beetles.

Figure 4

The effects of mites on burying beetle fitness, in relation to the beetle's size. (A) Proportion winning a contest against a medium‐sized female, in the presence or absence of mites (n = 40 small females and n = 37 large females). (B) Brood size at larval dispersal for small females and large females breeding in the presence or absence of mites (small females: n = 34 with mites and 33 without mites; large females: n = 33 with mites and 28 without mites). Means ± SE are shown. (C) Mean burying beetle fitness, calculated as the product of the mean probability of winning a contest (from A) and the mean number of larvae produced (from B), in relation to beetle size and the presence or absence of 30 mites.