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Allele specific expression and gene regulation help 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 potential to outperform native species. Effective management of hybrid populations requires an understanding of both physiological performance and the underlying mechanisms that drive transgressive hybrid traits. 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 F1 hybrids to tolerate acute thermal stress, and found that hybrids exhibit a wide range of CTMax values, with 33% (4/12) able to tolerate temperatures greater than either parent. We then quantified the genomic response, measured at the RNA transcript level, of each salamander, to explore the mechanisms underlying thermal tolerance strategies. We found that CTS and BTS have strikingly different values and tissue-specific patterns of overall gene expression, with hybrids expressing intermediate values. F1 hybrids display abundant and variable degrees of allele specific expression (ASE), likely arising from extensive compensatory evolution in gene regulatory mechanisms between CTS and BTS. We found evidence that the proportion of genes with allelic imbalance in individual hybrids correlates with their CTMax, suggesting a link between ASE and expanded thermal tolerance that may contribute to the success of hybrid salamanders in California. Future climate change may further complicate management of CTS if hybrid salamanders are better equipped to deal with rising temperatures.

ORGANISM(S): Ambystoma californiense

PROVIDER: GSE137607 | GEO | 2020/12/12

REPOSITORIES: GEO

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Project description:Study abstract: Axolotl salamanders (Ambystoma mexicanum) remain aquatic in their natural state, during which biomechanical forces on their diarthrodial limb joints are likely reduced relative to salamanders living on land. However, even as sexually mature adults, these amphibians can be induced to metamorphose into a weight-bearing terrestrial stage by environmental stress or the exogenous administration of thyroxine hormone. In some respects, this aquatic to terrestrial transition of axolotl salamanders through metamorphosis may model developmental and changing biomechanical skeletal forces in mammals during the prenatal to postnatal transition at birth and in the early postnatal period. To assess differences in the appendicular skeleton as a function of metamorphosis, anatomical and gene expression parameters were compared in skeletal tissues between aquatic and terrestrial axolotls that were the same age and genetically full siblings. The length of long bones and area of cuboidal bones in the appendicular skeleton, as well as the cellularity of cartilaginous and interzone tissues of femorotibial joints were generally higher in aquatic axolotls compared to their metamorphosed terrestrial siblings. A comparison of steady state mRNA transcripts encoding aggrecan core protein (ACAN), type II collagen (COL2A1), and growth and differentiation factor 5 (GDF5) in femorotibial cartilaginous and interzone tissues did not reveal any significant differences between aquatic and terrestrial axolotls. RNAseq samples: Total RNA was isolated from whole body tissue samples of Mexican axolotl salamanders (Ambystoma mexicanum) at the following developmental stages: Embryo at the tail bud stage, newly hatched larva, larva at the limb bud stage, juvenile at 8.5 centimeters, and adult using variations of guanidinium-based protocols. RNA quantity, purity, and integrity of both the individual samples and the resulting pool were determined with an Agilent 2100 Bioanalyzer using the Eukaryotic Total RNA nano series II analysis kit. The pooled RNA sample was poly-A selected and used for Illumina random priming directional library prep. Four lanes were sequenced only on one end providing single end reads and 4 lanes were sequenced at both ends giving paired-end reads. The library was sequenced on an Illumina HiSeq 2000 for 75bp reads producing 147,248,512 single end reads and 2 x 153,254,667 paired-end reads.

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

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