Within-generation and transgenerational social plasticity interact during rapid adaptive evolution

The role of within-generation phenotypic plasticity (WGP) versus transgenerational plasticity (TGP) during evolutionary adaptation are not well understood, particularly for socially-cued TGP. We tested how genetics, WGP, and TGP jointly influence expression of fitness traits facilitating adaptive evolution in the field cricket Teleogryllus oceanicus . A male-silencing mutation (“ flatwing” ) spread to fixation in ca. 50 generations in a Hawaiian cricket population attacked by acoustically-orienting parasitoids. This rapid loss of song caused the social environment to dramatically change. Juveniles carrying the flatwing ( fw ) genotype exhibited greater locomotive activity than those carrying the normal-wing ( nw ) allele, consistent with genetic coupling of increased locomotion with fw . Consistent with adaptive WGP, homozygous fw females developing in the absence of song showed reduced body condition and reproductive investment at adulthood. Adult but not juvenile offspring exhibited TGP in response to maternal social environment for structural size, somatic condition, and reproductive investment, whereas adult locomotion and flight was only influenced by WGP. WGP and TGP interacted to shape multiple traits at adulthood, though effect sizes were modest. Interactions between genetic effects and social plasticity within and across generations are likely to have influenced the evolutionary spread of flatwing crickets. However, interactions among these effects can be complex, and it is notable that TGP manifested most strongly later in development. Our findings stress the importance of evaluating trait plasticity at different developmental stages and across generations when studying phenotypic plasticity’s role in evolution.