Alien gene introgression promotes rapid adaptation: an unconscious experiment on Fire-bellied toad (Bombina bombina) at the northern edge of its distribution range
Final Report Abstract
Due to their isolated and often fragmented nature, range margin populations are especially vulnerable to rapid environmental change. To maintain genetic diversity and adaptive potential, gene flow from disjunct populations might therefore be crucial to their survival. Translocations are often proposed as a mitigation strategy to increase genetic diversity in threatened populations. However, this also includes the risk of losing locally adapted alleles through genetic swamping. Human-mediated translocations of southern lineage specimens into northern German populations of the endangered European fire-bellied toad (Bombina bombina) provided an unexpected experimental set up to test the genetic consequences of an intraspecific introgression from central population individuals into populations at the species range margin. Through the investigation of two candidate genes (MHC II and HSP70 kDa) for heterogeneity in the frequencies of introduced alleles, we detected lineage specific (northern vs. southern) genotypes and an expressed structural variation at the HSP locus exclusively for the southern lineage. Furthermore, the analyses of a variety of molecular markers (mitochondrial control region, mitochondrial genomes, MHC II, HSP70 kDa, transcriptome-wide SNPs) revealed a mosaic genomic structure in introgressed populations, meaning there are predominantly allochthonous genotypes/alleles found at some loci, but local alleles at others. Our project, investigating northern range margin B. bombina populations, shows that introgressive hybridization could increase the levels of genetic variation. These preliminary analyses indicate a putatively positive outcome for the affected populations. Locally adapted gene assemblages for MHC class II and HSP70 kDa have not been disrupted or replaced yet by an influx of foreign alleles. Instead, introgression has increased hybrid fitness in allochthonous northern populations, putatively caused by the influx of beneficial alleles at polygenic trait loci or their differential expression. Interestingly, interspecific hybridization between the fire bellied toad (B. bombina) and the yellow-bellied toad (B. variegata) has led to a fitness reduction in hybrids, which might be explained by different habitat preferences in both species or their divergent genomes. While B. bombina prefers lowland regions with larger, permanent ponds, B. variegata is mainly found in shallower, temporal water bodies at higher altitudes. Therefore, hybrids of both species might not be perfectly adapted to either of the parental habitats and suffer from outbreeding depression. Through genome-wide scans of 27 transcriptomes we uncovered signs of introgression in four out of the five northern populations investigated, including a number of introgressed alleles, ubiquitous in all recipient populations, suggesting a possible adaptive advantage. This was particularly apparent at the MTCH2 locus, associated with obesity/fat tissue in humans, and the DSP locus, essential for the proper development of epidermal skin in amphibians. Furthermore, we found loci where local alleles were retained in the introgressed populations, suggesting their relevance for local adaptation. Finally, comparisons of transcriptome-wide genetic diversity between introgressed and non-introgressed northern German populations revealed an increase in genetic diversity in all German individuals belonging to introgressed populations, supporting the idea of a beneficial transfer of genetic variation from Austria into North Germany. All in all, introgressive hybridization could represent a faster mechanism promoting rapid adaptation for the studied B. bombina populations. Novel, putatively adaptive de novo mutations may only occur at a slow rate relative to generation time and as the (standing) genetic variation in range margin populations of B. bombina is low, their future adaptive potential could be considered low. With introgressive hybridization present, selection would be able to act upon segregating blocks of genetic material instead of one or two new alleles generated by de novo mutation, which could be highly advantageous, especially when new ecological niches are created through a changing environment.
Publications
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(2019). The complete mitochondrial genome of a European fire-bellied toad (Bombina bombina) from Germany. Mitochondrial DNA Part B. 4: 498-500
De Cahsan, B., Westbury, M.V., Drews, H., Tiedemann, R.
