Fitness drivers of division of labor in vertebrates

Division of labor as a means to boost productivity holds significance not only in human societies, but also those of other animals ( Smith, 1776 ; Oster and Wilson, 1978 ; Dunbar et al., 2014 ; Zhang et al., 2016 ; Cooper and West, 2018 ). Nearly 250 years ago, the economist Smith, 1776 , proposed that division of labor via task specialization within human societies not only improves individual efficiency and group productivity, but also reduces the costs associated with switching tasks. Similarly, in nonhuman animal societies, division of labor to increase group reproductive output (analogous to economic gain) is characterized by group members specializing in particular tasks, either temporarily or permanently ( Michener, 1974 ; Beshers and Fewell, 2001 ; Jeanne, 2016 ;). To date, most theoretical and empirical work on the selective pressures favoring division of labor via task specialization in animal societies has focused on ‘classically’ eusocial insect societies characterized by permanently sterile workers that are never able to reproduce ( Wheeler, 1928 ; Wilson, 1971 ; Beshers and Fewell, 2001 ; Willensdorfer, 2009 ; Ispolatov et al., 2012 ; Li et al., 2025 ). Since workers in eusocial societies can, in most cases, only obtain fitness benefits indirectly through kin selection by maximizing their colony reproductive output, selection can occur at the colony level, typically resulting in very low conflict of interest between group members. However, complex societies occur outside of eusocial insects, such as in many birds and mammals, including humans. Because sterile workers are absent in vertebrates and other cooperative breeding societies, conflict can be much higher than in most eusocial insect societies. The few studies of division of labor outside of eusocial insects have primarily focused on reproductive division of labor (i.e. reproductive skew), despite that fact that temporal or permanent non-reproductive organisms can engage in an array of different helping tasks ( Cooper and West, 2018 ; Yanni et al., 2020 ; Taborsky et al., 2025 ). Given the scarcity of studies examining the selective advantages of division of labor beyond eusocial insects (but see Ridley and Raihani, 2008 ), our understanding of the evolutionary pressures of division of labor is largely confined to instances where task specialization is linked to sterility and where conflict of interest is generally low ( Wenseleers et al., 2021 ).

In cooperatively breeding vertebrates, which typically live in societies with more equitable sharing of reproduction than eusocial insects (i.e. low reproductive skew), low or mixed kinship, and often have unrelated helpers, conflict of interest can be high, and direct fitness benefits may be more relevant in the evolution of division of labor than indirect benefits ( Dunn et al., 1995 ; Doutrelant et al., 2011 ; Riehl, 2013 ). In fact, shared fitness incentives to increase group productivity are not limited to eusocial insects with high within-group relatedness and sterile workers. In cases where group size positively correlates with an increase in the survival or reproduction of group members, division of labor via task specialization may also evolve under direct fitness benefits to subordinate members of a group (i.e. group augmentation; Kokko et al., 2001 ; Kingma et al., 2014 ). Although a great deal of recent empirical work highlights the importance of direct benefits in the evolution of cooperative breeding behavior in vertebrates ( Richardson et al., 2002 ; Sparkman et al., 2011 ; Zöttl et al., 2013b ; Shah and Rubenstein, 2023 ), we still lack an understanding of the joint influence of direct and indirect fitness benefits in the evolution of division of labor.

Understanding how direct and indirect benefits interact is particularly important in systems where individuals may differentially bear the fitness costs of cooperation. Most previous models of division of labor via task specialization considered all helping tasks under the same fitness umbrella, which is a good approximation in eusocial insect societies because colony members share fitness costs and benefits. In vertebrates and social insects with fertile workers, however, helpers may obtain fitness benefits directly via reproduction, and thus, selection occurs more strongly at the individual level than it does in most eusocial insects. Group members in vertebrate societies may then contribute to distinct helping tasks differently according to individual life-history strategies ( Cockburn, 1998 ; Anderson, 2001 ; Beehner and Kitchen, 2007 ) or differences in the magnitude or type of fitness costs and benefits that they receive from cooperative tasks ( Nunn and Lewis, 2001 ). One of the key distinctions between fitness costs is whether a task impacts more immediate survival or direct reproduction. For instance, defensive behaviors such as predator mobbing may have a high risk of injury and death ( Poiani and Yorke, 1989 ; Sordahl, 1990 ; Tórrez et al., 2012 ), whereas other activities such as allofeeding or nest/territory maintenance may affect body condition owing to lower feeding rates and time and energy investment, consequently affecting individual reproductive output ( Heinsohn and Cockburn, 1994 ; Grantner and Taborsky, 1998 ; Heinsohn and Legge, 1999 ). Therefore, changes in life histories, such as those linked to the likelihood of becoming a breeder, may select for task specialization according to the relative direct fitness cost associated with different helping tasks.

In addition to life-history differences, demographic, social, and ecological factors that affect helper workload and the prospect of helpers becoming breeders are likely to have a strong impact on task allocation because they alter the probability of obtaining direct fitness benefits ( Young et al., 2005 ; Zöttl et al., 2013a ). For example, age is known to be an important factor influencing helping workload in vertebrates ( Komdeur, 1996 ; Boland et al., 1997 ), is often correlated with differences in other life-history traits ( Heinsohn and Cockburn, 1994 ; Taborsky, 1984 ; Boesch, 2002 ; Clutton-Brock et al., 2003 ), and may be a proxy for other processes involved in the evolution of help ( Johnstone and Cant, 2010 ; Fischer et al., 2014 ). Moreover, age-dependent task allocation (i.e. temporal polyethism) is common in eusocial insects that do not show morphological differentiation ( Hölldobler and Wilson, 1990 ). Social and ecological factors are also thought to influence the emergence of division of labor in eusocial insects ( Sendova-Franks and Franks, 1993 ; Traniello and Rosengaus, 1997 ; Ferguson-Gow et al., 2014 ). Indeed, high relatedness may reduce conflict of interest between group members and promote the evolution of division of labor ( Queller and Strassmann, 1998 ; Gardner and Grafen, 2009 ; Keller and Chapuisat, 2010 ; Fisher et al., 2013 ; West et al., 2015 ). Similarly, in harsh environments where group size strongly influences survival ( Rood, 1990 ; Clutton‐Brock et al., 1999 ; Taborsky et al., 2005 ; García-Ruiz and Taborsky, 2022 ), division of labor may be favored to more efficiently increase group productivity.

To disentangle the role of direct versus indirect fitness benefits in the evolution of division of labor in cooperative breeding societies with totipotent helpers, we created an individual-based model in which we varied the influence of different evolutionary forces to understand social and ecological circumstances under which division of labor may arise to maximize the inclusive fitness of individuals in a group. We used distinct tasks with different fitness costs to maximize the group reproductive output when they were performed to a similar extent. Individuals in our model were allowed to evolve different behavioral responses or reaction norms in task specialization, depending on their probability of becoming breeders. We compared the results of this model to those of a benchmark model in which the reproductive outcome was independent of the type of task performed by group members. We present the results for different environmental conditions in the presence or absence of relatedness (indirect) or group size (direct) benefits. Ultimately, this work demonstrates that the direct fitness benefits of group living attained in increasingly harsh environments are key to the evolution of division of labor in vertebrates.

Our findings suggest that the direct benefits of group living play a driving role in the evolution of division of labor via task specialization in species with totipotent workers, including all vertebrates and a few insects. In contrast, in eusocial species characterized by high relatedness and permanent worker sterility, such as in most eusocial insects, workers acquire fitness benefits only indirectly, and so, their fitness is contingent upon the overall success of the colony rather than the individual ( Foster et al., 2006 ; Hughes et al., 2008 ). Group members in such eusocial species are therefore predicted to maximize colony fitness due to the associated lower within-group conflict and to favor the evolution of division of labor to increase group productivity efficiency ( Gardner and Grafen, 2009 ; Fisher et al., 2013 ; West et al., 2015 ). However, in taxa with lower within-group relatedness, such as nearly all vertebrates, division of labor is facilitated when cooperation is crucial for survival and when the benefits of cooperation are evenly distributed among group members ( Cooper and West, 2018 ). In particular, survival fitness benefits derived from living in larger groups seem to be key for the evolution of cooperative behavior in vertebrates ( García-Ruiz et al., 2022 ; Shah and Rubenstein, 2023 ;), and may also translate into low within-group conflict. This suggests that selection for division of labor in vertebrates is stronger in smaller groups, where increased productivity significantly enhances survival, as opposed to research on eusocial insects that posits division of labor is more likely to evolve in larger groups ( Dornhaus et al., 2012 ; Nakahashi and Feldman, 2014 ; Ulrich et al., 2018 ). That is not to say, however, that kin selection is unimportant in cooperatively breeding vertebrates or insects. Our model demonstrates that cooperative breeders are more likely to evolve division of labor when direct and indirect fitness benefits act in concert. Moreover, our model predicts that the type of task that individuals prefer depends on the type of fitness benefit that subordinates can attain. While direct fitness benefits in the form of group augmentation select more strongly for defensive tasks, kin selection alone seems to select only for work tasks. In groups of unrelated individuals where members can only gain direct fitness benefits, costs to dominance value and to the probability of attaining a breeding position are comparatively larger than survival costs. Conversely, groups with no group benefits tend to be small and suffer high mortality, for which defensive tasks only aggravate the situation.

Previous models of task allocation in eusocial insects have focused on how seemingly identical individuals of the same age and broad morphology may specialize in different types of tasks ( Ulrich et al., 2018 ; Beshers and Fewell, 2001 ). In contrast, our model shows that extrinsic ecological factors are also important for the evolution of task specialization in addition to intrinsic factors such as age or dominance rank. In short, our model predicts that task specialization, which varies with age or rank, will depend on environmental quality. In more favorable environments, helpers are predicted to increase defensive tasks with age or rank, whereas in harsh environments, work tasks are predicted to increase with age or rank. Furthermore, harsher environments exert stronger selective pressure for task specialization due to increased survival challenges. Enhanced cooperation and improved group productivity through helping mitigate the negative effects of the environment. This finding is consistent with previous research on the role of ecological constraints in driving the evolution of cooperation ( Emlen, 1982 ; Hatchwell and Komdeur, 2000 ; Kokko and Ekman, 2002 ).

Although rare, evidence of division of labor in cooperative breeding vertebrates comes from a few studies in mammals ( Lacey and Sherman, 1996 ), birds ( Arnold et al., 2005 ; Ridley and Raihani, 2008 ), and fishes ( Bruintjes and Taborsky, 2011 ; Josi et al., 2020 ). Our model predictions are broadly consistent with empirical data from many of these studies. For example, support for the role of environmental harshness on the evolution of division of labor via age-dependent task specialization in vertebrates comes from arguably the most similar vertebrate system to eusocial insects, the naked mole-rat ( Heterocephalus glaber ). Naked mole-rats live in self-dug burrows that protect their inhabitants from predation and climatic extremes ( Lacey and Sherman, 1996 ). Therefore, even though they inhabit habitats with scarce and unpredictable rainfall, environmental harshness is likely to be limited in their stable subterranean burrows, with mortality mainly spiking during dispersal attempts. Model predictions for species that evolved in benign environments are then met, with individuals shifting from work tasks such as foraging for food, digging, and maintaining the burrow system, to defensive tasks such as guarding and patrolling as individuals grow older and larger ( Faulkes et al., 1991 ; Lacey and Sherman, 1996 ; Lacey and Sherman, 2017 ). Although naked mole-rats exhibit high levels of within-colony relatedness ( Reeve et al., 1990 ), group size also exerts a positive influence on survival, potentially generating group augmentation benefits ( O’Riain and Braude, 2001 ; le Comber et al., 2002 ). Under these conditions, our model predicts the highest levels of task partitioning and division of labor. In contrast, Neolamprologus pulcher , a cooperatively breeding cichlid fish that lives in harsh environments with high risk of predation ( Taborsky, 2016 ), shows the opposite tendency. In line with our model predictions, larger and older helpers of this species invest relatively more in territory maintenance, whereas younger/smaller helpers defend the breeding shelter of the dominant pair to a greater extent against experimentally exposed egg predators ( Bruintjes and Taborsky, 2011 ). Territory maintenance has been shown to greatly affect routine metabolic rates and, hence, growth rates ( Taborsky and Grantner, 1998 ), which directly translates into a decrease in the probability of becoming dominant and attaining breeding status. In addition, both group augmentation and kin selection have been found to play a role in the evolution of help in this species ( Zöttl et al., 2013b ; García-Ruiz and Taborsky, 2022 ). More research is needed to verify whether this trend is widespread in cooperatively breeding vertebrates with division of labor. The preferred form of help provided by individuals throughout their life course might deviate from our expectations if helpers exhibit differing abilities to perform distinct tasks at different ages or life stages. We assumed that individuals of all ages possessed equal capability to perform different tasks. However, as individuals age and their size and body mass increase, they may become more adept at certain tasks such as deterring predators ( Brown, 1985 ; Heinsohn and Cockburn, 1994 ; Clutton-Brock et al., 2002 ; Woxvold et al., 2006 ; Zahed et al., 2010 ; Erb and Porter, 2020 ). Body condition that is unrelated to age may also influence helper contributions, as individuals in poorer condition may be more constrained on their energy allocation in activities other than self-maintenance ( Clutton-Brock et al., 2000 ; Clutton-Brock et al., 2001 ; Nichols et al., 2012 ). Furthermore, our model does not capture instances in which help in general or specific tasks are enforced by the dominant pair or other more dominant group members ( Kokko et al., 2002 ; Hellmann and Hamilton, 2018 ; García-Ruiz and Taborsky, 2024 ).

Despite evidence of task specialization and division of labor across several vertebrate taxa, other empirical studies have failed to find similar results. For instance, researchers failed to find evidence of task specialization in Damaraland mole-rats ( Fukomys damarensis ), despite their social structure resembling that of naked mole-rats ( Zöttl et al., 2016 ; Thorley et al., 2018 ), with some variation in digging behavior with age and sex ( Rotics et al., 2025 ). However, it is worth noting that researchers have only investigated correlates between different work tasks, potentially overlooking negative correlations with other helping activities that pose a more direct cost to survival. In fact, many studies that reported an absence of division of labor did not consider defensive tasks in their analyses ( English et al., 2010 ; Zöttl et al., 2016 ; Thorley et al., 2018 ; Smith et al., 2024 ). Nonetheless, studies exist in which researchers did not find a negative correlation between defense and offspring provisioning or territory maintenance ( Clutton-Brock et al., 2003 ; van Asten et al., 2016 ; Teunissen et al., 2020 ). However, individuals may exhibit a positive or non-relationship between tasks if they also vary in total helpfulness across their lifetime, but may still switch the proportion of time/effort allocated to different types of tasks. In our model, we addressed for this potential tendency by restricting individuals from changing their overall helpfulness with age/dominance rank. We encourage future researchers to consider the proportion of time/energy investment in addition to examining correlations between tasks.

In summary, our study helps to elucidate the potential mechanisms underlying division of labor between temporal non-reproductives via task specialization in taxa beyond eusocial organisms. Harsh environments, where individuals can obtain direct fitness benefits from group living, favor division of labor, thereby enhancing group productivity and, consequently, group size. Variation in the relative fitness costs of different helping tasks with age favors temporal polyethism, with individuals changing their behavior patterns to improve their chances of becoming breeders. Hence, future empirical research on division of labor should prioritize cooperatively breeding species inhabiting relatively harsh environments where subordinates benefit greatly from group membership, such as protection or improved food acquisition. Additionally, we emphasize the importance of including sentinel and defense behaviors in future studies to encompass a broader spectrum of fitness costs of cooperation and to investigate potential changes in task investment throughout the helpers’ lifetimes.

We developed an individual-based model in which individuals may display and vary their efforts in different helping tasks. The ancestral state features an absence of alloparental care and no task specialization. We assume that residing in larger groups yields overall survival advantages, potentially resulting in direct fitness benefits associated with the increase in group size, as proposed by the group augmentation hypothesis. We also include the coevolution of the helping strategies with their dispersal propensity, as dispersal affects group size and kin structure, and thus may impact the strength of indirect fitness benefits.

Custom code used to generate the simulations is available at (copy archived at García-Ruiz, 2026 ).

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Author details

1. Irene García-Ruiz

   Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, United States

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Funding acquisition, Visualization, Methodology, Writing – original draft

   For correspondence

   igaru.13@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6139-5857

2. Dustin R Rubenstein

   Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, United States

   Contribution

   Supervision, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4999-3723

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