The whale shark genome reveals how genomic and physiological properties scale with body size
Jessica A. Weber, Seung Gu Park, Victor Luria, Sungwon Jeon, Hak-Min Kim, Yeonsu Jeon, Youngjune Bhak, Je Hun Jun, Sang Wha Kim, Won Hee Hong, Semin Lee, Yun Sung Cho, Amir Karger, John W. Cain, Andrea Manica, Soonok Kim, Jae-Hoon Kim, Jeremy S. Edwards, Jong Bhak, and George M. Church
Significance
We sequenced and analyzed the genome of the endangered whale shark, the largest fish on Earth, and compared it to the genomes of 84 other species ranging from yeast to humans. We found strong scaling relationships between genomic and physiological features. We posit that these scaling relationships, some of which were remarkably general, mold the genome to integrate metabolic constraints pertaining to body size and ecological variables such as temperature and depth. Unexpectedly, we also found that the size of neural genes is strongly correlated with lifespan in most animals. In the whale shark, large gene size and large neural gene size strongly correlate with lifespan and body mass, suggesting longer gene lengths are linked to longer lifespans.
Abstract
The endangered whale shark (Rhincodon typus) is the largest fish on Earth and a long-lived member of the ancient Elasmobranchii clade. To characterize the relationship between genome features and biological traits, we sequenced and assembled the genome of the whale shark and compared its genomic and physiological features to those of 83 animals and yeast. We examined the scaling relationships between body size, temperature, metabolic rates, and genomic features and found both general correlations across the animal kingdom and features specific to the whale shark genome. Among animals, increased lifespan is positively correlated to body size and metabolic rate. Several genomic traits also significantly correlated with body size, including intron and gene length. Our large-scale comparative genomic analysis uncovered general features of metazoan genome architecture: Guanine and cytosine (GC) content and codon adaptation index are negatively correlated, and neural connectivity genes are longer than average genes in most genomes. Focusing on the whale shark genome, we identified multiple features that significantly correlate with lifespan. Among these were very long gene length, due to introns being highly enriched in repetitive elements such as CR1-like long interspersed nuclear elements, and considerably longer neural genes of several types, including connectivity, activity, and neurodegeneration genes. The whale shark genome also has the second slowest evolutionary rate observed in vertebrates to date. Our comparative genomics approach uncovered multiple genetic features associated with body size, metabolic rate, and lifespan and showed that the whale shark is a promising model for studies of neural architecture and lifespan.
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