Paternal programming in sticklebacks

Abstract

In a wide range of organisms, including humans, mothers can influence offspring via the care they provide. Comparatively little is known about the effects of fathering on offspring. Here, we test the hypothesis that fathers are capable of programming their offspring for the type of environment they are likely to encounter. Male threespine sticklebacks, Gasterosteus aculeatus, were either exposed to predation risk while fathering or not. Fathers altered their paternal behaviour when exposed to predation risk, and consequently produced adult offspring with phenotypes associated with strong predation pressure (smaller size, reduced body condition, reduced behavioural activity). Moreover, more attentive fathers produced offspring that showed stronger antipredator responses. These results are consistent with behaviourally mediated paternal programming: fathers can alter offspring phenotypes to match their future environment and influence offspring traits well into adulthood.

A female's past experience with predators affects male courtship and the care her offspring will receive from their father

“…For example, threespined stickleback fathers reduce their paternal care when presented with a predator model [26]. Interestingly, the way males in this study reduced their paternal care in response to female past experience with predation risk is strikingly similar to the way males reduce paternal care in response to their own (direct) experience with predation risk [26]. Examining whether males reduce their reproductive investment when females have been exposed to stressors other than predators (e.g.…”

“…For example, offspring might be 'programmed' for high predation risk by mothers via their pre-fertilization provisioning into eggs [21] and by fathers via adjustments to offspring care [26]. This would, in part, explain why maternal predator exposure results in maladaptive offspring behaviour when offspring are reared without care (as orphans [13]) and experience a 'mismatch' between maternal and paternal cues of high predation risk.…”

“…Thus, previous predator experiences of mothers can influence offspring traits and survival both directly [12,13,21] and indirectly through how these experiences affect paternal care (this study). Paternal care in this species affects offspring behavioural [26,28,29] and morphological [26] development, brain gene expression [28] and is linked to offspring survival with predators [28]. Whether paternal care can compensate for the negative effects of maternal predator exposure on offspring, or complements these maternal effects, remains unknown.…”

Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety

“…In sticklebacks, there is evidence that fathers tend to be consistent across breeding attempts [26]. However, an encounter with a model predator while caring for offspring can have consequences for offspring behaviour and morphology suggesting that offspring development might be altered by subtle shifts in father behaviour [16]. The covariation between parent and offspring behaviour could also be environmentally induced (i.e.…”

“…During this period, offspring rely on yolk reserves provisioned by their mother prior to fertilization. Fathers do not feed offspring, but there is evidence that offspring antipredator behaviour [14], mate preference [15] and morphology [16] can be sensitive to the effects of fathers.…”