Genetic detection and population structure of a non-native hybridogenic Poeciliopsis species in the Santa Cruz River of Arizona, USA

Abstract

The Gila topminnow (Poeciliopsis occidentalis) has undergone population recovery actions since being extirpated from much of its historical range in the United States of America (USA) prior to the 1970s. However, it returned to the Santa Cruz River in 2015 independently of these actions, which prompted concerns that a non-native Poeciliopsis lineage had been introduced from Mexico. Some Gila topminnow populations in Mexico are sympatric with P. monacha-occidentalis, which is an exclusively female taxon that originated from historical hybridization between P. occidentalis and headwater livebearer (P. monacha). This hybrid taxon reproduces through hybridogenesis, which is a unique mode of sexual reproduction in which half of one parent’s genome is inherited without recombination. This unique property was leveraged to identify hybridogens among 868 individuals from Arizona, USA using common genetic markers (i.e., nuclear microsatellite and mitochondrial sequence data). We described methods for P. monacha-occidentalis identification and conducted population genetic analysis of Santa Cruz River P. occidentalis populations to infer their possible origins. We concluded that human-mediated introduction was the most probable explanation for the current Santa Cruz River P. occidentalis and P. monacha-occidentalis presence. Contemporary diversity may be explained by four introduction events. Population ancestry estimates indicate that P. monacha-occidentalis may have hybridized with two P. occidentalis lineages in the Santa Cruz River. Variable prevalence of P. monacha-occidentalis was noted in two river sections, but the conservation implications of this hybridization are unclear. Public education, targeted removal of P. monacha-occidentalis, and genetic monitoring could mitigate future introductions and potential negative impacts.