About the Study:
Global environmental changes have a profound impact on the evolution of species, shaping their characteristics, distribution, and survival strategies. In particular, the rapid uplift and climate changes of the Qinghai-Tibet Plateau (QTP) have significantly influenced modern biological diversification since the early Cenozoic era. A few species have been found to spread out of the QTP region driven by intense climate changes during the Quaternary Ice Age (2.6Ma-present). However, these species could experience different fates after a long-term evolutionary process as they encountered various challenges arising from low-altitude environments. Unfortunately, little was known about the drivers of evolution and adaption for these organisms. Parnassius butterflies have the largest genome among all members of Papilionidae. Among them, Parnassius glacialis is a typical "Out of the QTP" alpine butterfly that originated on the QTP and dispersed into relatively low-altitude mountainous of East Asia with larger body size. In this study, we assembled a chromosome-level genome of P. glacialis and resequencde 9 populations in order to explore the pattern of genome evolution and local adaptation for this species. Through a series of comparative genomic analyses, we discovered that transposable elements (TEs) play an important role in genomic evolution and local adaptation of P. glacialis spreading out of the QTP.
We discovered that Parnassius species at low elevations had relatively larger genome sizes compared to those at high elevations. The genome size of most species on the QTP is ranged from 1.0 Gb to 1.2 Gb, but that of a few species (e. g. P. glacialis) outside the QTP is generally between 1.27-1.4 Gb. Through further comparison of genomic compositions, we found that the rapid accumulation and slow unequal recombination of transposable elements (TEs) contributed to the formation of P. glacialis’ large genome. These mobile elements (TEs) have been active to mediate a few of ribosome gene duplications (e. g. the acidic ribosomal P protein (RPLP)). Funny enough, 434 RPLP2 genes were identified in P. glacialis, while only one or two RPLP2 genes were found in the other butterfly species. These RPLP2 genes presented rapid evolution since about 3 Ma during the early Quaternary Ice Age, which was generally consistent with the timing of TEs activity in P. glacialis. Most RPLP2 genes exhibited processed pseudogene features (such as intron absence, start codon loss, or early coding termination), only a few of them obtained the start codons and displayed normal expression as the functional genes. Moreover, we discovered that the P. glacialis populations at high altitudes near the QTP have higher genetic diversity and larger population size than the low-altitude populations far away from the QTP under the trend of global warming after the Last Glacial Maximum (LGM, 26.5–19 ka). Concurrently, genome regions with transposon-mediated structural variation (TE-SVs) were found to harbor lower recombination rate and higher FST values than those without, indicating that TE activity probably tended to increase the genetic differentiation between high- and low-altitude P. glacialis populations. Furthermore, a series of genes with selective signature were identified for the low-altitude population, enriching in several pathways associated to the function of antioxidant, development and immune. These genes with selective signature harbor significantly more TE-SVs than that of others without signature. These results suggested that TE-SVs might provide more opportunities for selective evolution of P. glacialis to meet challenges (such as oxidative damage, higher atmospheric pressure, new competitors or predators, and invasion of pathogenic microorganism in warmer regions) of new habitats outside the QTP.
Why It Matters:
In summary, the Quaternary Ice Age played a pivotal role in shaping the evolutionary trajectories of animals. The selective pressures imposed by glacial and interglacial cycles prompted the development of diverse adaptations, influencing the composition and distribution of life on Earth. Our research suggests that TEs may have a crucial role in genome evolution, including genome size variation, processed pseudogene expansion, population genetic differentiation and potential local adaptation for P. glacialis during this period. These findings open new insights for the drivers of evolution and adaptation for alpine organisms spreading out of the QTP.
Read the Full Manuscript:
For those interested in a deeper dive, the full manuscript is now available on Nature Communications: https://doi.org/10.1038/s41467-023-44023-2