Retention of low-fitness genotypes over six decades of admixture between native and introduced tiger salamanders

Abstract

BackgroundIntroductions of non-native tiger salamanders into the range of California tiger salamanders have provided a rare opportunity to study the early stages of secondary contact and hybridization. We produced first- and second-generation hybrid salamanders in the lab and measured viability among these early-generation hybrid crosses to determine the strength of the initial barrier to gene exchange. We also created contemporary-generation hybrids in the lab and evaluated the extent to which selection has affected fitness over approximately 20 generations of admixture. Additionally, we examined the inheritance of quantitative phenotypic variation to better understand how evolution has progressed since secondary contact.ResultsWe found significant variation in the fitness of hybrids, with non-native backcrosses experiencing the highest survival and F2 hybrids the lowest. Contemporary-generation hybrids had similar survival to that of F2 families, contrary to our expectation that 20 generations of selection in the wild would eliminate unfit genotypes and increase survival. Hybrid survival clearly exhibited effects of epistasis, whereas size and growth showed mostly additive genetic variance, and time to metamorphosis showed substantial dominance.ConclusionsBased on first- and second- generation cross types, our results suggest that the initial barrier to gene flow between these two species was relatively weak, and subsequent evolution has been generally slow. The persistence of low-viability recombinant hybrid genotypes in some contemporary populations illustrates that while hybridization can provide a potent source of genetic variation upon which natural selection can act, the sorting of fit from unfit gene combinations might be inefficient in highly admixed populations. Spatio-temporal fluctuation in selection or complex genetics has perhaps stalled adaptive evolution in this system despite selection for admixed genotypes within generations.

Long-term experimental hybrid swarms between moderately incompatible Tigriopus californicus populations: hybrid inferiority in early generations yields to hybrid superiority in later generations

“…It lends support to the notion that outbreeding depression may be a temporary phenomenon (Templeton 1986;Rieseberg et al 1996;Carney et al 2000;Christiansen 2008; but see also Johnson et al 2010) and offers a ray of hope for managers faced with situations where the introduction of genetically divergent individuals may be the only remaining option to bolster a dwindling population. Managers should focus efforts on assessing whether the mixing of populations is likely to result in hybrid persistence or genetic swamping, as results from an additional study show that the amount of divergence between the populations at hand, and the fitness of the individual populations in a particular environment, may have a large influence on the outcome of hybridization (Hwang et al in prep).…”

Conservation Genetics and Genomics of Amphibians and Reptiles

“…In a series of papers, our laboratory has demonstrated that nonnative A. t. mavortium introduced into central California in the 1950s led to the formation of a hybrid swarm in approximately 25% of the range of the federally and state-protected California tiger salamander (A. californiense); another 25% has been invaded by a smaller set (3/68 marker loci) of superinvasive genes that are spreading more rapidly (46,59,60). At both the phenotypic and genetic levels, these hybrids generally have higher fitness than pure native salamanders, raising serious conservation concerns for the endangered A. californiense (61)(62)(63)(64).…”

Population-level genetic variation and climate change in a biodiversity hotspot

“…When introgression accompanies hybridization, dilution of the native gene pool can occur (Abbott, 1992;Johnson JR et al, 2010;Johnson MG et al, 2016), and can result in extinction of the native species (Anttila et al, 1998). Often underrated, human-mediated hybridization is one of the leading causes of biodiversity loss via homogenization of formerly distinct populations or taxa (Muhlfeld et al, 2009).…”