Energetic Benefits of Sociality Offset the Costs of Parasitism in a Cooperative Mammal

Heike Lutermann,John R Speakman,Michael Scantlebury,Nigel C Bennett,Gabriele Sorci

doi:10.1371/journal.pone.0057969

Abstract

Sociality and particularly advanced forms of sociality such as cooperative breeding (living in permanent groups with reproductive division of labour) is relatively rare among vertebrates. A suggested constraint on the evolution of sociality is the elevated transmission rate of parasites between group members. Despite such apparent costs, sociality has evolved independently in a number of vertebrate taxa including humans. However, how the costs of parasitism are overcome in such cases remains uncertain. We evaluated the potential role of parasites in the evolution of sociality in a member of the African mole-rats, the only mammal family that exhibits the entire range of social systems from solitary to eusocial. Here we show that resting metabolic rates decrease whilst daily energy expenditure and energy stores (i.e. body fat) increase with group size in social Natal mole rats (Cryptomys hottentotus natalensis). Critically, larger groups also had reduced parasite abundance and infested individuals only showed measurable increases in energy metabolism at high parasite abundance. Thus, in some circumstances, sociality appears to provide energetic benefits that may be diverted into parasite defence. This mechanism is likely to be self-reinforcing and an important factor in the evolution of sociality.

Highlights

The energy costs of parasitism are presumed to arise as a result of the physiological consequences of mounting an immune response, the costs of repairing tissue damage and/or direct resource competition with the host [1,2,3,4]
We tested the suggestion that sociality generates energetic benefits which offset the cost of parasitism by measuring the resting metabolic rate (RMR) and cestode abundance of wild Natal mole-rats of different colony sizes
Similar negative relationships between group size and parasite burden have been shown for directly transmitted ectoparasites and this has been attributed to increased allo-grooming rates with group size [27,31]

Summary

Introduction

The energy costs of parasitism are presumed to arise as a result of the physiological consequences of mounting an immune response, the costs of repairing tissue damage and/or direct resource competition with the host [1,2,3,4]. We tested the suggestion that sociality generates energetic benefits which offset the cost of parasitism by measuring the resting metabolic rate (RMR) and cestode abundance (i.e. the mean number of parasites per individual) of wild Natal mole-rats of different colony sizes. We hypothesized that larger colony sizes would be associated with energetic benefits If these benefits reduce metabolic costs we predicted that DEE would decrease with colony size whilst fat stores would be increased in larger colonies. This might offset the elevated costs of parasitism leading to no overall relationship between group size and daily energy demands

Results

Discussion

Findings

Materials and Methods