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

Abstract

Background: Introductions 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.

Results: We 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.

Conclusions: Based 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.

Figure 1

Comparison of line - cross means to weighted expected mean survival in the 0th (solid line), 1st (dashed line), and 2nd (dotted line) generations of admixture (± 95% CI). The 'Source Index' (θS) = 2P - 1, where P is the average frequency of introduced BTS alleles in each cross type (Lynch 1991).

Figure 2

Box-and-whisker plots of phenotypic trait values for A) Mass, B) SVL, C) Tmet, & D) Growth. Mass and SVL have been log-transformed and Tmet and Growth have been square-root-transformed. Letters above each line cross denote significant differences at α = 0.05 based on multiple t-test comparisons with Bonferroni correction. Horizontal lines denote the expected mean phenotypes for contemporary hybrids in the 0th (solid line segment), 1st (dashed line segment), and 2nd (dotted line segment) generations of admixture. The abbreviation 'Cont. Hyb.' stands for 'Contemporary Hybrids'.