Environment-Dependent Admixture Dynamics in a Tiger Salamander Hybrid Zone

Abstract

After an estimated five million years of independent evolution, the barred tiger salamander (Ambystoma tigrinum mavortium) was introduced by bait dealers into the native range of the California tiger salamander (A. californiense). Hybridization and backcrossing have been occurring in central California for 50-60 years, or an estimated 15-30 generations. We studied genetic and ecological factors influencing admixture of these two divergent gene pools by analyzing frequencies of hybrid genotypes in three kinds of breeding habitats: natural vernal pools, ephemeral man-made cattle ponds, and perennial man-made ponds. Perennial ponds tended to have higher frequencies of nonnative alleles than either type of seasonal pond, even in cases where perennial and seasonal ponds are within a few hundred meters. Thus, the hybrid zone has a mosaic structure that depends on pond hydrology or ecology. The presence of some broadly acting constraints on admixture is suggested by linkage disequilibria between physically unlinked molecular markers within ponds. In addition, we found several marker-specific deviations from Hardy-Weinberg equilibrium. One marker showed a consistent deficit of heterozygotes across pond types. Another showed heterozygote deficits only in vernal pools. A third was more likely to have heterozygote excess in ephemeral cattle ponds. These patterns indicate that admixture is influenced by complex genotype-by-environment interactions.

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

“…Localized environment-dependent admixture dynamics have previously been reported in this hybrid swarm [35], with perennial ponds supporting more introduced ( i.e ., higher HIS or θ S ) populations. We have also reared a small number (N = 50) of other contemporary hybrids from a perennial site (Johnson Canyon Landfill; JCL) with a HIS of 0.81 near the Pond H contemporary hybrid site.…”

“…Furthermore, avoiding the semi-arid, and often highly agricultural terrestrial habitat that has typified the hybrid swarm region since the initial BTS introduction 60 years ago may further increase fitness of paedomorphic ( i.e ., permanently aquatic) salamanders. Life-history factors have been hypothesized to promote the invasion success of BTS (and BTS-like hybrids) in perennial ponds, where they seem to have a distinct advantage in the field [35]. In the laboratory and the field [27], F1 individuals appear unable to take full advantage of long-hydroperiod aquatic resources by extending the larval growth period, suggesting that fitness gains associated with artificial, perennial breeding sites were not important in the initial success of F1 hybrids.…”

“…Although CTS populations readily exchange individuals [56,57], previous genetic surveys of other populations near the Pond H contemporary hybrid population [33,35,36,38] suggest that there are few if any pure CTS populations remaining that could balance the effect of viability selection for increasing introduced allele frequency. On the other hand, these genetic surveys demonstrate that highly nonnative individuals exist in close proximity to our contemporary hybrid site.…”

“…While there have been many generations of admixture in the heart of the Salinas Valley hybrid swarm, there has not been enough time for any nonnative allele to become fixed throughout the range of the native species [34]. Furthermore, the success of hybrid genotypes appears heavily influenced by local environmental conditions, with anthropogenic changes in breeding habitat supporting increasingly non-native admixed populations [35,36]. …”

Do relaxed selection and habitat temperature facilitate biased mitogenomic introgression in a narrowly endemic fish?

“…For instance, it is possible that the putatively more cold‐adapted H. cyanoguttatus is better able to breed in colder habitats leading to the observed preponderance of their mitochondria in these springs. These possibilities could be explored using field studies of survivorship and observations of breeding in different springs in Cuatro Ciénegas (Fitzpatrick and Shaffer 2004; Chunco 2014; Chown et al. 2015).…”