Differences in Cooperative Behavior Among Damaraland Mole Rats Are Consequences of an Age-Related Polyethism

Differences in cooperative behavior among Damaraland mole rats are consequences of an age-related polyethism Markus Zöttla,1, Philippe Vulliouda, Rute Mendonçab,c, Miquel Torrents Ticóa,d, David Gaynorb, Adam Mitchelld, and Tim Clutton-Brocka,b aDepartment of Zoology, University of Cambridge, Cambridge CB23EJ, United Kingdom; bDepartment of Zoology and Entomology, Mammal Research Institute, University of Pretoria, 0028 Pretoria, South Africa; cInstitute of Biology, University of Neuchatel, Rue Emile-Argand 11, CH-2000 Neuchatel, Switzerland; and dKalahari Mole-Rat Project, Kuruman River Reserve, 8467 Van Zylsrus, South Africa Edited by Joan E. Strassmann, Washington University in St. Louis, St. Louis, MO, and approved July 6, 2016 (received for review May 17, 2016) In many cooperative breeders, the contributions of helpers to variation in cooperative behavior is age-related (18, 19). An im- cooperative activities change with age, resulting in age-related portant difference is that castes are permanent, functionally dif- polyethisms. In contrast, some studies of social mole rats (includ- ferent, and discrete groups of individuals that differ in behavior, ing naked mole rats, Heterocephalus glaber, and Damaraland mole physiology, or morphology and hence castes represent highly rats, Fukomys damarensis) suggest that individual differences in specialized strategies, whereas variation caused by age-related cooperative behavior are the result of divergent developmental polyethisms remains plastic throughout development (refs. 20, 21, pathways, leading to discrete and permanent functional cate- “narrow sense caste” in the sense of ref. 22). gories of helpers that resemble the caste systems found in eusocial This study investigates whether the distribution of labor in insects. Here we show that, in Damaraland mole rats, individual Damaraland mole rats is the result of an age-related polyethism contributions to cooperative behavior increase with age and are or whether there is evidence of the formation of castes and of higher in fast-growing individuals. Individual contributions to dif- permanent differences in behavior between frequent and infre- ferent cooperative tasks are intercorrelated and repeatability of quent workers, as has been suggested in previous studies of na- cooperative behavior is similar to that found in other coopera- ked mole rats (13, 17) and Damaraland mole rats (14). tively breeding vertebrates. Our data provide no evidence that Distinguishing a system of specialized workers that are organized nonreproductive individuals show divergent developmental path- in castes [in the sense of Michener (21)] from an age-related ways or specialize in particular tasks. Instead of representing a polyethism requires longitudinal records of behavior and growth caste system, variation in the behavior of nonreproductive individ- of known-aged individuals. A caste system, as suggested for so- uals in Damaraland mole rats closely resembles that found in other cial mole rats, would predict that (i) behavioral phenotypes of cooperatively breeding mammals and appears to be a consequence individuals with different growth trajectories diverge during on- of age-related polyethism. togeny; (ii) the behavioral profiles of individuals are related to their asymptotic body mass rather than their age; (iii) the distribution of cooperative behavior shows a bi- or multimodal division of labor | eusociality | caste | cooperative breeding | distribution; (iv) individuals specialize permanently in certain social mole rats tasks, so that some forms of cooperative behavior show negative correlations among individuals; and that (v) repeatability of n cooperatively breeding vertebrates and primitively eusocial Iinsects, subordinate group members frequently vary widely in Significance their investment in cooperative tasks. These differences are often consequences of state-dependent changes in fitness costs and benefits, which vary with age, growth, and sex (1–6), and result in Nonreproductive group members of naked and Damaraland age- and sex-related polyethisms where behavior varies in relation mole rats are thought to be organized in permanent, distinct to opportunities to breed. In cooperatively breeding meerkats castes that differ in behavior and physiology, suggesting that (Suricata suricatta) for example, fast growing helpers contribute their social organization resembles that of obligatorily eusocial more to overall cooperative behavior; supplementary feeding in- insects. This study tests predictions about the distribution of creases help; and subordinates do not specialize in certain tasks (3, cooperative behavior based on the suggestion that individual 4, 7). Similar patterns are widespread among other cooperative differences represent a caste system. Our data provide no evi- breeders from diverse taxa [birds (8), mammals (9), fish (10, 11), dence that helpers show fixed, divergent developmental path- and primitively eusocial insects (5, 6)]. ways or specialize in particular tasks. Instead, variation in their It has been suggested that naked mole rats (Heterocephalus behavior appears to represent an age-related polyethism. The glaber) and Damaraland mole rats (Fukomys damarensis) are an results suggest that the behavioral organization of social mole- exception to this pattern (12–14). In these species, the main rat groups is similar to that of other singular cooperatively cooperative task performed by nonbreeding helpers (building a breeding vertebrates, and that similarities to obligatorily large network of foraging tunnels) is primarily carried out by eusocial insects have been overestimated. small individuals of both sexes (12, 14–17) and it has been argued previously that this may be the result of a caste system, similar to Author contributions: M.Z., P.V., R.M., and T.C.-B. designed research; M.Z., P.V., R.M., M.T.T., those found in some eusocial insect species. Some studies suggested D.G., and A.M. performed research; M.Z. analyzed data; and M.Z. and T.C.-B. wrote that in mole rats, specialized, smaller workers conduct most of the the paper. energetically demanding burrowing and remain in this state for their The authors declare no conflict of interest. entire life, whereas larger workers contribute little to cooperative This article is a PNAS Direct Submission. burrowing but specialize in other cooperative tasks, including nest Data deposition: Data reported in this paper have been deposited in the Figshare re- building, alloparental care, or colony defense (12, 14). Others have pository (dx.doi.org/10.6084/m9.figshare.3570987). argued that it is premature to assume that naked mole rats show a 1To whom correspondence should be addressed. Email: [email protected]. caste system because the observed differences in behavior could be This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. the result of age-related polyethisms, as it is not clear whether 1073/pnas.1607885113/-/DCSupplemental. 10382–10387 | PNAS | September 13, 2016 | vol. 113 | no. 37 www.pnas.org/cgi/doi/10.1073/pnas.1607885113 Downloaded by guest on September 30, 2021 cooperative behavior through ontogeny is high. Alternatively, an (Fig. 1A and Table 1, total cooperation). Males and females with age-related polyethism based on state-dependent costs and stra- high residual body mass (i.e., fast-growing individuals) invested tegic resource allocation contingent on opportunities to breed more in cooperative behavior than individuals with low residual would predict that (i) cooperative investment changes with age; body mass during the first year of their life, but this relationship (ii) asymptotic body mass is not necessarily related to cooperative reversed in the second year when females with low residual body behavior; (iii) cooperative behavior is continuously distributed; mass showed higher investment in cooperative behavior than (iv) individuals do not specialize in certain activities so that there males or females with high residual body mass (interaction: sex × are positive correlations in their investment in different coopera- residual body mass × age) (Fig. 1A and Table 1, total cooperative tasks; and (v) cooperative investment should be contingent on tion). Across nonreproductive individuals older than 600 d but an individual’s state and life history, which frequently results in a bias toward the more philopatric sex and toward fast-growing with unknown exact age, body mass did not predict investment in cooperative behavior (Fig. 1B) [generalized linear mixed model individuals. = − = = Our study tests these predictions about the distribution of (GLMM): body mass: estimate 0.07, P 0.18; sex: estimate cooperative behavior based on the suggestion that individual 0.11, P = 0.34, n = 644 observations of n = 75 individuals in differences represent a caste system or an age-related polyethism 13 groups]. Asymptotic body mass of known-aged individuals using behavioral data, collected under controlled laboratory (derived from a Gompertz growth function) was also unrelated conditions on 187 nonreproductive Damaraland mole rats from to investment in summed cooperative behavior after the age of 37 colonies between the ages of 60 and 600 d and 75 nonre- 300 d (GLMM, asymptotic body mass, estimate = 0.02, P = 0.63, productive individuals from 13 colonies, which were older than n = 122) and in all age categories, frequency distribution of total 600 d but whose exact age was unknown. Damaraland mole rats cooperation across individuals showed

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