REVIEW: CAUSES AND CONSEQUENCES OF DOING IT WITH ONESELF-SYNTHESIS AND META-ANALYSIS OF NEODERMATAN HERMAPHRODITIC MATING SYSTEMS.

Abstract

Hermaphroditic mating systems profoundly influence evolution, yet in parasitic flatworms (Neodermata) they remain strikingly understudied. For decades, sweeping claims have oscillated between pervasive selfing and near-universal outcrossing, reflecting a lack of comprehensive synthesis. This review, the first in more than 40 yr, integrates nearly a century of research, from early observational studies to modern genetic analyses, to reveal a far more nuanced picture. Our meta-analysis of population-genetic data shows a sharp departure from the bimodal selfing patterns typical of plants and other hermaphroditic animals: neodermatan parasites are strongly skewed toward outcrossing. We link variation in mating systems to parasite demography and life-history traits, especially in species exhibiting mixed mating or elevated selfing. Current evidence suggests outcrossing is common, but taxonomic and life-history gaps preclude definitive conclusions. Beyond patterns and causes, we explore evolutionary consequences ranging from fitness costs such as inbreeding depression to trait evolution, including delayed selfing, sex allocation, and complex life cycles. Evidence for inbreeding depression is mixed and limited, yet emerging approaches using selfing-rate comparisons offer promising avenues for future research. Notably, demographic constraints, such as infection intensity and life-cycle architecture, often explain mixed mating without invoking selection, challenging classical models. Similarly limited in number, studies on sex allocation indicate that hermaphroditic mating systems can shape reproductive investment, with patterns consistent with local sperm competition in some taxa. By consolidating historical observations with modern genetic insights, this review provides the most comprehensive synthesis of hermaphroditic mating systems in the Neodermata to date. We highlight critical gaps in taxonomic coverage and experimental data and point to future opportunities for integrating genomic approaches with ecological and demographic frameworks. Such integration will be essential to illuminate how mating systems shape parasite evolution and to resolve long-standing questions about the persistence of mixed mating despite theoretical expectations.