Maternal effects in cooperative breeders: from hymenopterans to humans

Abstract

The environment that an offspring experiences during its development can have lifelong consequences for its morphology, anatomy, physiology and behaviour that are strong enough to span generations. One aspect of an offspring's environment that can have particularly pronounced and long-lasting effects is that provided by its parent(s) (maternal effects). Some disciplines in biology have been quicker to appreciate maternal effects than others, and some organisms provide better model systems for understanding the causes and consequences of the maternal environment for ecology and evolution than others. One field in which maternal effects has been poorly represented, and yet is likely to represent a particularly fruitful area for research, is the field of cooperative breeding (i.e. systems where offspring are reared by carers in addition to parent(s)). Here, we attempt to illustrate the scope of cooperative breeding systems for maternal effects research and, conversely, highlight the importance of maternal effects research for understanding cooperative breeding systems. To this end, we first outline why mothers will commonly benefit from affecting the phenotype of their offspring in cooperative breeding systems, present potential strategies that mothers could employ in order to do so and offer predictions regarding the circumstances under which different types of maternal effects might be expected. Second, we highlight why a neglect of maternal strategies and the effects that they have on their offspring could lead to miscalculations of helper/worker fitness gains and a misunderstanding of the factors selecting for the evolution and maintenance of cooperative breeding. Finally, we introduce the possibility that maternal effects could have significant consequences for our understanding of both the evolutionary origins of cooperative breeding and the rise of social complexity in cooperative systems.

Figure 1

Summary of the ecological causes and evolutionary consequences of maternal effects considered. Maternal effects can be passive or active (Badyaev 2005). Passive effects are likely to be common in all animal systems; here we concentrate on active maternal strategies and effects which we believe are likely to be particularly important in cooperative systems. The two most important factors selecting for active maternal effects will be ecological heterogeneity and the strength and predictability of the relationship between maternal strategy and fitness. If there is no ecological heterogeneity or a weak and/or unpredictable relationship between maternal strategy and fitness, active maternal effects will not be expected. The strength and extent of maternal effects will be further modified by the dynamics of mother–offspring conflict. Greater selection on maternal effects might be expected where maternal strategies and offspring strategies do not converge and where offspring have considerable scope for counteracting a given maternal strategy. Strong maternal effects will in turn further influence ecological heterogeneity, leading to positive feedback between each, again modified by the dynamics of maternal-offspring conflict. Finally, while within-generation maternal effects can be strong without inheritance, ultimately evolutionary change will become more likely when maternal effects are inherited, either epigenetically or genetically.

Figure 2

Hypothetical models for the evolution of cooperative breeding and the rise of complexity with (a) maternal control and (b) offspring control. In situation (a), consider offspring fitness is enhanced more by staying at home than maternal fitness, e.g. because of ecological constraints on breeding. If mothers never tolerate offspring or cannot resist offspring, offspring always leave or stay without helping, respectively. Cooperative breeding will evolve if maternal toleration is enhanced by offspring evolving cooperation. Mothers have four options in response to helpful offspring. If maternal tenure is predictable and maternal fitness is enhanced by producing high-quality offspring (as is likely in ecological constraints), mothers would benefit most from option (A) and/or (B) (bold lines). This could lead to a conflict of interest because helpers will often benefit from mothers producing many, low-quality offspring (i.e. option C) since such offspring will themselves have reduced outside options and so stay in the group, compete less for reproduction within the group and lighten the load of the helper. In addition, option C might allow helpers to maximize indirect fitness while waiting for an opportunity to breed (Gadakar 1990). However, mothers are in control and will evict offspring that counters the most adaptive maternal strategy. Thus, although cooperative breeding can evolve through this scenario, complexity is unlikely to arise, because there is little selection on mothers increasing current fecundity and hence group size, which is the precursor to increasing complexity (Bourke 1999). In scenario (b), mothers would benefit from having offspring that stay at home and help while offspring would benefit from dispersing to breed. Maternal effects are likely to be instrumental in achieving helpful offspring in the first place. In order to retain offspring, mothers can either offer them staying incentives (path 1) or ‘control’ them by reducing their outside options (path 2, table 2). Staying incentives can be either direct (1E) or indirect (1F). Direct staying incentives (in the form of shared reproduction) are unlikely to be stable because no individual can gain control and cooperative systems are thus likely to either break down or remain simple. Indirect staying incentives (in the form of indirect fitness benefits from helping kin) would lead to offspring gaining the upper hand because they would simply leave if mothers were not able to provide them with sufficient scope for gaining indirect fitness. All else being equal, sufficient scope is likely to arise in the form of increased current fecundity, which in turn could lead to selection for further helpers, further increases in group size and potentially an increase in complexity (obviously depending on constraints on group size and maternal fecundity). However, the evolvability of this route is unclear. Maternal control (path 2) of offspring will be best achieved by honest under-investment, since if under-investment is dishonest, offspring will be selected to procure withheld resources. Honest under-investment can arise if mothers increase current fecundity (owing to quality–quantity trade-offs). Under maternal control of offspring, mothers in the presence of helpers have the same four options as in (a) (here 2A–D), but this time mothers might already be committed to path 2C, since their ability to achieve helpful offspring in the first place is reliant upon having high fecundity. If mothers attempt any of the other three routes, offspring will be reared in good condition and will subsequently disperse (because offspring are ultimately in control).