Multigenerational effects of microplastics and phthalates on fitness-related traits in a field cricket

Global plastic production is increasing exponentially, making microplastics (MPs; plastic particles <5 mm) ubiquitous in animals' environments. Microplastics can exhibit sex-specific toxicity and release harmful phthalate esters (PAEs), which are known endocrine disruptors in vertebrates and are often added to plastics to enhance flexibility and durability. Yet, we lack a comprehensive understanding of the combined biological effects of MPs and PAEs. Because environments exhibit long-term contamination by MPs and PAEs, maternal and paternal exposure to these contaminants may have carryover (transgenerational) effects on offspring. Here, we used a factorial design with dietary MPs and PAEs in the variable field cricket (Gryllus lineaticeps) to determine within-generation effects on reproduction (mating success and egg production) and across-generation effects on offspring (e.g., hatching success and hatchling developmental rates). Exposure to PAEs during early adulthood entailed significant within- and across-generational costs, including reduced parental mating success and reduced offspring hatching success, respectively. Adults exposed to PAEs also had offspring with altered developmental life histories characterized by a shortened embryonic stage and a prolonged post-embryonic stage. In contrast, the within- and across-generational effects of maternal and paternal MPs exposure were context-dependent and only evident through certain interactions. For example, MPs and PAEs interacted in a context-dependent antagonistic dynamic where exposure to one of these factors improved egg-laying, whereas exposure to both factors eliminated the observed benefit. In sum, we show that plastic pollution- particularly, PAEs- pose comprehensive threats to animals spanning from generation to generation.