Allele specific expression and gene regulation explain transgressive thermal tolerance in non-native hybrids of the endangered California tiger salamander (Ambystoma californiense)

Abstract

Hybridization between native and non-native species is an ongoing global conservation threat. Hybrids that exhibit traits and tolerances that surpass parental values are of particular concern, given their ability to outcompete the native parent. It is crucial to understand the mechanisms that drive these transgressive hybrid traits to diagnose and develop strategies to manage hybrid populations. Here, we explore several aspects of the hybridization between the endangered California tiger salamander (Ambystoma californiense; CTS) and the introduced barred tiger salamander (Ambystoma mavortium; BTS). We assayed critical thermal maximum (CTMax) to compare the ability of CTS, BTS and hybrids to tolerate acute thermal stress, and found that hybrids exhibit a wide range of CTMax values, with 40% (6/15) able to tolerate temperatures greater than either parent. We quantified the genomic response of each individual to discover and compare thermal abatement strategies. We found that CTS and BTS have strikingly different numbers and tissue-specific patterns of overall gene expression, with hybrids expressing intermediate values. We evaluated transgressive and variable phenotypes by uncovering regulatory mechanisms that give rise to these unique traits. F1 hybrids display abundant and variable degrees of allele specific expression (ASE), likely arising from extensive compensatory evolution in gene regulatory mechanisms of the parental lineages. We found that the proportion of genes with allelic imbalance in individual hybrids correlates with their CTMax, suggesting that BTS-biased expression confers improved thermal tolerance. We discuss the implications of these findings with respect to ongoing management of CTS in the face of future climate change.

Morphometry of two cryptic tree frog species at their hybrid zone reveals neither intermediate nor transgressive morphotypes

“…Stabilizing selection, genetic drift, or varying selective regimes in the evolutionary history may promote the evolution of transgressive loci, while consistent selective regimes may favor the accumulation of alleles with steady effects (Albertson & Kocher, 2005; Orr, 1998). At immediate contact, epigenetic factors may be contributing to the occurrence and thus evolution of transgressive patterns seen in hybridizing lineages (Cooper & Shaffer, 2021 incl. refs.…”

Managing invasive hybrids through habitat restoration in an endangered salamander system

“…To even quantify the presence of hybridization often requires sophisticated genomic tools. Estimating its impact often requires field-based ecological experiments to evaluate fitness, both in absolute terms and compared to the native parental lineages that are being replaced (21, 25, 31, 33). If hybrids are viewed as a conservation threat, as has been the case in many systems, the most vexing challenge is the final step—how to differentially reduce or eliminate non-native alleles from an admixed hybrid swarm, or at least slow the advance of non-native introgression in the wild.…”

“…Coupled with the apparent increase in fitness from elevated heterozygosity inherent in hybrids (68), this may have produced the transgressive 'hopeful monsters' (73) that exceed the fitness of native CTS, as has been demonstrated in thermal tolerance (31).…”

“…Fitzpatrick et al (30) modeled the dynamics of hybrid zone expansion and found that non-native alleles reach fixation much faster than is expected based on neutral diffusion models. Other studies have documented hybrid superiority in thermal tolerance (31), locomotor performance (32), and water-quality tolerance (33). This evidence predicts that hybrid salamanders will eventually replace native CTS at least regionally, resulting in genome-level extinction (34).…”

Concern over hybridization risks should not preclude conservation interventions

“…Further complicating the answer, Cooper and Shaffer (2019) found that CTS/BTS hybrids are more flexible in their abilities to tolerate thermal extremes than pure CTS, suggesting that hybrids may be better suited to a warming climate. While hybridization is, by definition, a threat to the “genetic integrity” of CTS, it may also be a path to the long‐term survival of many of its genes on the California landscape.…”