The whale shark genome reveals how genomic and physiological properties scale with body size

Abstract

The endangered whale shark (Rhincodon typus) is the largest fish on Earth and is 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 81 animals and yeast. We examined 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 features also significantly correlated with body size, including intron and gene length. Our large-scale comparative genomic analysis uncovered general features of metazoan genome architecture: 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 large introns highly enriched in repetitive elements such as CR1-like LINEs, and considerably longer neural genes of several types, including connectivity, activity, and neurodegeneration genes. The whale shark's genome had an expansion of gene families related to fatty acid metabolism and neurogenesis, with the 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. 4The relationships between body mass, longevity, and basal metabolic rate (BMR) across diverse habitats and taxa have been researched extensively over the last century, and led to generalized rules and scaling relationships that explain many physiological and genetic trends observed across the tree of life. While studies of endothermic aquatic mammals have shown that selection for larger body sizes is driven by the minimization of heat loss 1 , metabolic rate in ectothermic aquatic vertebrates is directly dependent on temperature, and decreased temperatures are correlated with decreased BMRs, decreased growth rates, longer generational times, and increased body sizes 2-4 . The whale shark (Rhincodon typus) is the largest extant fish, reaching lengths of 20 meters (m) 5 and 42 tonnes (t) in mass 6 and has a maximum lifespan estimated at 80 years 6 . Unlike the two smaller filter-feeding shark species (Cetorhinus maximus, Megachasma pelagios) that inhabit colder temperate waters with increased prey availability, whale sharks have a cosmopolitan tropical and warm subtropical distribution and have rarely been sighted in areas with surface temperatures less than 21°C 7-9 . However, recent GPS tagging studies have revealed that they routinely dive to mesopelagic (200-1,000 ...

The whale shark genome reveals patterns of vertebrate gene family evolution

“…Despite their large body size, endangered status, and appeal to both scientists and the general public, relatively little is known about their biology [8][9][10] . Due to its phylogenetic position among vertebrates, the scarcity of shark genomes, and its unique biology, the whale shark genome can be used to address questions related to vertebrate genome evolution 11,12 , the relationship of gene evolution in sharks and unique shark traits 11,12 , as well as the evolution of gigantism 13 . As expected, Read et al found that whale shark genome was most closely related among sequenced fish genomes (at the time) to Callorhinchus .…”

“…More recent work has focused upon further sequencing, assembling, and analyzing of the whale shark nuclear genome 6,11,13 . Hara et al 11 generated novel elasmobranch genome assemblies for the brown-banded bamboo shark ( Chiloscyllium punctatum ) and cloudy catshark ( Scyliorhinus torazame ).…”

“…They also reassembled the published Read et al whale shark genome data, supplementing it with transcriptome sequence from blood cells sampled from a different male individual. Their comparative genomic study confirmed a reduced evolutionary rate in cartilaginous fish genomes 11 , a conclusion previously drawn from only a handful of genes 14,15 . Park et al 13 then reported on a whale shark genome assembly from a third male individual and compared genomic characteristics from animals to yeast to identify correlates of longevity and genome traits. They found that much of the increase in the gene length in the whale shark genome was due to relatively large introns that were enriched for CR1-like LINEs.…”