Genome evolution of Suidae: a looking glass of speciation and hybridization
Understanding the origin of species and biodiversity is one of the fundamental objectives in evolutionary biology. Continuous efforts to sequence additional species have generated a comprehensive dataset for biologists to explore the underlying biological mechanisms contributing to evolution and to aid conservation of ecosystems. The aim of my thesis is to utilize genome scale data to provide new insight into the evolutionary process and mechanisms in Suidae evolution. In this work, I provided a comprehensive view of the evolutionary history of pig species, spanning from species origin to current time. Furthermore, the refined comparative genomic framework of Suidae species contributes to our understanding of the effects of complex speciation and hybridization from an evolution genomics perspective.In Chapter 2 we sequenced and analyzed the genomes of the highly endangered pygmy hog (Porcula salvania). Phylogenetic reconstructions using whole-genome data strongly support pygmy hog as a distinct genus separated from other Suinae species, whereby the controversial taxonomic classification is resolved. Time of divergence estimation suggested that pygmy hog initially emerged during the Miocene/Pliocene boundary some 5.1 million years ago. Moreover, admixture analyses revealed at least two independent events of inter-species gene flow during wild boar range expansion across Eurasia. Despite the large phylogenetic divergence, wild boar interbred with pygmy hog and a now-extinct species which exhibit a deep phylogenetic placement between pygmy hog and warthog. Our analyses highlight the important role of admixture as evolutionary biological driving force in successful range expansion and species replacement.In Chapter 3 we provided an in-depth analysis of the formation of the current pygmy hog population and demonstrated consequences of the historical demography. Using whole genome sequencing data of six individual pygmy hogs, our demographic analysis revealed that pygmy hog has remained at small population sizes with low genetic diversity since ~1 Mya. The absence of mitochondrial variation in the six sequenced individuals suggested a historical maternal bottleneck. Runs of homozygosity (ROH) analysis showed that pygmy hog does not comprise high ROH coverage and long ROH, indicating very little recent inbreeding. Also, our genome wide scan and simulation of harmful mutations suggested that the long-term, extremely small population size may have constrained the purifying effect and led to the accumulation of genetic load.In Chapter 4 we generated a Sus cebifrons (the Visayan warty pig) genome assembly using linked-read sequencing and chromosome conformation capture techniques. The assembly is on chromosome level, which consisting of 17 chromosomes and yielding a genome size of 2.48 Gb and scaffold N50 of 141.8 Mb. The alignment of the Sus cebifrons assembly and Sus scrofa assembly (Duroc - Sscrofa11.1) revealed a high degree of collinearity, but also chromosome fission and fusion. The comparison of chromosome interaction maps suggested that, due to the short divergence time between Visayan warty pig and Duroc pig (~3 Mya), the chromosome 3D conformation structure remained the same after the chromosomal rearrangements. We hypothesized that this may explain the absence of post-zygotic reproductive isolation among Sus species. We further identified the different signatures of adaptive and domestication selection in Visayan warty pig and domestic pig, respectively. In particular, we investigated the evolution of olfactory and gustatory genes and reported the genetic basis of species-specific sensation.In Chapter 5 we went one step further and used a reference-guided assembly approach to generate genome sequences for three other Sus species (i.e., Sus verrucosus, Sus celebensis and Sus barbatus) and the outgroup species Porcula salvania. With the near complete phylogenomic framework of Sus species, we were able to perform admixture analyses directly from genome sequences. This unbiased admixture analysis reaffirmed the extensive inter-species gene flow between Sus is concomitant with past climatic fluctuations. In addition, we tested the shift of selection pressure along the Sus phylogeny and interpreted the results in the context of paleobiogeographic evidence. We provided candidate genes that might have contributed to adaptive radiation and domestication of pigs. This case study demonstrates that utilizing genome sequences is a powerful tool for evolutionary and functional genomic analyses.Finally, in Chapter 6, I string all chapters together and provide additional discussion on the findings presented in Chapter 2 to 5. I discuss the molecular and genetic mechanism underlying the complex evolutionary history of Suidae species. I also discuss the evolution of genome architecture during speciation and hybridization from a general perspective. Lastly, I summarize methodological challenges of evolutionary analysis in the genomic era and explore the potential implication of the emerging methods.
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| Format: | Doctoral thesis biblioteca |
| Language: | English |
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Wageningen University
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| Subjects: | Life Science, |
| Online Access: | https://research.wur.nl/en/publications/genome-evolution-of-suidae-a-looking-glass-of-speciation-and-hybr |
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