Nongenetic inheritance of behavioural variability is context specific and sex specific

Environmentally mediated nongenetic inheritance extends the concept of phenotypic plasticity across generations, allowing for the experience of parents to influence the physiology, life history and behaviour of their offspring. We assess whether the perceived social environment of mothers and fathers impacts offspring behaviour in the Australian field cricket Teleogryllus oceanicus. We varied parents' perception of the density of conspecific males by exposing parents to either the presence or absence of male song throughout rearing. Following mating in a factorial design, the offspring of the parental pairs were also reared across the two acoustic environments and their behaviour assessed as adults. When reared in a no-song environment, offspring of both sexes were more active, emerging from a shelter sooner and displaying greater mobility in search of male song. Offspring behaviour was not directly impacted by either the maternal or paternal social environments independently, but there was a significant interaction effect between the parental environments on the behaviour of daughters. When both parents were reared in song (‘paternal song × maternal song’), their no-song-reared daughters exhibited lower levels of mobility than the no-song-reared daughters of ‘paternal song × maternal no-song’ and ‘paternal no-song × maternal song’ pairs. Although our data suggest that nongenetic parental effects may have the potential to drive behavioural variability in offspring, such effects are highly complex, only arising as sex- and context-specific traits. A free Plain Language Summary can be found within the Supporting Information of this article.