Effects of parental care on the accumulation and release of cryptic genetic variation: review of mechanisms and a case study of dung beetles

Cryptic genetic variation plays an important role in the emergence of disease and evolutionary responses to environmental change. Focusing on parental care behavior, we discuss three mechanisms by which behavior can affect the accumulation and release of cryptic genetic variation. We illustrate how these hypotheses might be tested with preliminary data from Onthophagus dung beetles, which provide indirect parental care by provisioning their offspring with dung and sheltering them underground. The environmental stress hypothesis states that parental care reduces selection intensity on novel mutations when increased parental care results in a less stressful offspring environment. A review of recent literature, coupled with an irradiation experiment in beetles, suggests this mechanism may operate in some situations, but depends on the types of mutations under consideration. The relaxed selection hypothesis states that genes expressed in low care environments should be under weakened selection because their phenotypic manifestations are exposed to selection less frequently, and thus are prone to mutation accumulation. If parental care is reduced, for instance due to population-wide environmental changes, such cryptic variation may exert phenotypic effects, becoming exposed to selection. There is substantial theory in support of this hypothesis, and comparisons between beetle populations that differ in parental care behavior further support this idea. Finally, the compensation hypothesis states that organisms with direct parental care may be able to respond to cues or signals from offspring and compensate for genetic variants. We highlight the extensive discussion of this hypothesis with respect to medical care and genetic load in humans and explore invertebrate systems that may constitute powerful models for further inquiry. In summary, several mechanisms exist by which care behavior may shape the accumulation and release of cryptic genetic variation, thereby affecting the potential emergence of diseases and the rate and direction of evolutionary responses to novel environments.