The Role of Hybrid Vigor in the Replacement of Pecos Pupfish by Its Hybrids with Sheepshead Minnow

Abstract

Many species are jeopardized by hybridization and genetic introgression with closely related species.Unfortunately, the mechanisms that promote or retard gene flow between divergent populations are little studied and poorly understood. Like many imperiled fish species, the Pecos pupfish (Cyprinodon pecosensis) is threatened with replacement by its hybrids with a close congener. We examined swimming performance and growth rate of hybrid pupfish to determine the role of hybrid vigor in the genetic homogenization of C. pecosensis by its hybrids with sheepshead minnow (C. variegatus). The F1 hybrids, backcross hybrids, and purebred C. variegatus displayed greater swimming endurance than purebred C. pecosensis. In addition, F1 hybrids and C. variegatus grew more rapidly than C. pecosensis. The ecological superiority of hybrids probably promoted their rapid spread through and beyond the historic range of C. pecosensis. These results indicate that eradication of hybrids and restoration of C. pecosensis to its native range is unlikely. Extinction of unique species via genetic homogenization can result from human activities that increase gene flow between historically fragmented populations; conservation managers must weigh the potential for such a catastrophe against the presumed benefits of increased interpopulation gene flow. This example illustrates how, after hybridization has occurred, conflict may arise between formerly complementary conservation goals.El Papel de Vigor Híbrido en el Reemplazo de Cyprinodon pecosensis por Sus Híbridos con C. variegatus Resumen: Muchas especies están en peligro por hibridación e introgresión genética con especies cercanamente relacionadas. Desafortunadamente, los mecanismos que promueven o retardan el flujo génico entre poblaciones divergentes son poco estudiados y comprendidos. Como muchas especies de peces en peligro,Cyprinodon pecosensis está amenazada con reemplazo por sus híbridos con un congénere cercano. Examinamos el desempeño natatorio y la tasa de crecimiento de peces híbridos para determinar el papel del vigor híbrido en la homogenización genética de C. pecosensis por sus híbridos con C. variegatus. Los híbridos F1, los híbridos de retrocruza y C. variegatus puros mostraron mayor resistencia natatoria que C. pecosensis puros. Adicionalmente, los híbridos F1 y C. variegatus crecieron más rápidamente que C. pecosensis. La superioridad ecológica de híbridos probablemente promovió su rápida dispersión dentro y más allá del rango histórico de C. pecosensis. Estos resultados indican que la erradicación de híbridos y la restauración de C. pecosensis en su rango nativo es poco probable. La extinción de especiesúnicas por vía de homogenización genética puede ser resultado de actividades humanas que incrementan el flujo génico entre poblaciones históricamente fragmentadas; los gestores de conservación deben sopesar el potencial de tal catástrofe con los supuestos beneficios

Reproductive isolation and the expansion of an invasive hybrid swarm

“…Our work suggests that heterosis, possibly in conjunction with interspecific competition, is contributing to the expansion of the C. lutrensis x C. venusta hybrid swarm in the Coosa River basin (Walters et al 2008) and that assortative mating delayed the onset of hybridization following secondary contact. In contrast, heterosis and preferential choice of male sheepshead minnow (Cyprinodon variegatus) by female Pecos pupfish (C. pecosensis) fueled the replacement of Pecos pupfish by hybrids throughout more than half of the species' range in less than 5 years (Echelle and Connor 1989;Wilde and Echelle 1992;Childs et al 1996;Rosenfield and Kodric-Brown 2003;Rosenfield et al 2004). Although these examples illustrate a plausible trend, further reviews and direct tests will be necessary for more precise understanding of the relationship between the pace of invasions and reproductive isolation (Suehs et al 2006).…”

“…If so, then factors impeding species recognition but not courtship cues could be responsible for promoting hybridization between introduced red shiner and native congeners (Hankison and Morris 2002). It is also possible that interspecific competition is promoting hybridization since aggression can dictate the outcome of malemale competition for spawning territory (KodricBrown and Rosenfield 2004). Greater fecundity in red shiner females compared to blacktail shiner females could also promote hybridization because factors that alter the relative frequency of cross-compatible species can affect levels of hybrid production (Field et al 2008).…”

“…Rosenfield and Kodric-Brown 2003;Rosenfield et al 2004;Suehs et al 2006;Ayres et al 2008) suggest the onset of aggressive spread varies according to the strength of sexual isolation between native and non-native congeners. Intrinsic hybrid fertility (Sloop et al 2009) and hybrid vigor (Vilá and D'Antonio 1998;Rosenfield et al 2004;Walters et al 2008) also appear to be common elements of invasions that exhibit remarkable rates of advance. Our work suggests that heterosis, possibly in conjunction with interspecific competition, is contributing to the expansion of the C. lutrensis x C. venusta hybrid swarm in the Coosa River basin (Walters et al 2008) and that assortative mating delayed the onset of hybridization following secondary contact.…”

“…Both prezygotic and postzygotic isolating mechanisms can impede or promote the formation and persistence of hybrids (Coyne and Orr 2004), but knowledge of reproductive isolation between native and non-native species is weighted towards understanding postzygotic factors that may promote widespread invasion (Ellstrand and Schierenbeck 2000;Sakai et al 2001;Lee 2002). Few comparisons of prezygotic and postzygotic isolation have been carried out that contextualize the relevance of postzygotic conditions (Rosenfield and Kodric-Brown 2003;Rosenfield et al 2004;Kodric-Brown and Rosenfield 2004;Suehs et al 2006;Ayres et al 2008).…”

Rapid spread of invasive genes into a threatened native species

“…Other studies of hybridization between native and introduced species have documented replacement of native gene pools by admixed or even predominantly introduced genotypes (4,12,(37)(38)(39)(40). Demographic imbalances between domestic and wild populations might create asymmetrical gene flow and deterministic spread of selectively neutral or even deleterious alleles (41).…”