Complementary evolution of coding and noncoding sequence underlies mammalian hairlessness.

Body hair is a defining mammalian characteristic, but several mammals, such as whales, naked mole-rats, and humans, have notably less hair. To find the genetic basis of reduced hair quantity, we used our evolutionary-rates-based method, RERconverge, to identify coding and noncoding sequences that evolve at significantly different rates in so-called hairless mammals compared to hairy mammals. Using RERconverge, we performed a genome-wide scan over 62 mammal species using 19,149 genes and 343,598 conserved noncoding regions. In addition to detecting known and potential novel hair-related genes, we also discovered hundreds of putative hair-related regulatory elements. Computational investigation revealed that genes and their associated noncoding regions show different evolutionary patterns and influence different aspects of hair growth and development. Many genes under accelerated evolution are associated with the structure of the hair shaft itself, while evolutionary rate shifts in noncoding regions also included the dermal papilla and matrix regions of the hair follicle that contribute to hair growth and cycling. Genes that were top ranked for coding sequence acceleration included known hair and skin genes Whales, elephants, humans, and naked mole-rats all share a somewhat rare trait for mammals: their bodies are covered with little to no hair. The common ancestors of each of these species are considerably hairier which must mean that hairlessness evolved multiple times independently. When distantly related species evolve similar traits, it can be interpreted as a certain aspect of their evolution repeating itself. This process is called ‘convergent evolution’ and may provide insights about how different species were able to arrive at the same outcome. One possibility is that they have undergone similar genetic changes such as turning on or off key genes that play a role in the trait’s development. Kowalczyk et al. set out to identify what genetic changes may have contributed to the convergent evolution of hairlessness in unrelated species of mammals. By looking at the genomes of 62 mammalian species, they hoped to link specific genomic elements to the origins of the hairless trait. The genetic sequences under investigation included nearly 20,000 genes that encode information about how to make proteins, as well as 350,000 regulatory sequences composed of non-coding DNA, which specify when and how genes are activated. This marks the first time genetic mechanisms behind various hair traits have been studied in such a diverse group of mammals. Using a computational approach, Kowalczyk et al. identified parts of the genome that have evolved similarly in mammalian species that have lost their hair. They found that genes and regulatory sequences, that had been previously associated with hair growth, accumulated mutations at significantly different rates in hairless versus hairy mammals. This indicates that these regions associated hair growth are also related to evolution of hairlessness. This includes several genes that encode keratin proteins, the main material that makes up hair. The team also reported an increased rate of evolution in genes and regulatory sequences that were not previously known to be involved in hair growth or hairlessness in mammals. Together these results suggest that a specific set of genetic changes have occurred several times in different mammalian lineages to drive the evolution of hairlessness in unrelated species. Kowalczyk et al. describe the parts of the genome that may be involved in controlling hair growth. Once their findings are validated, they could be used to develop treatments for hair loss in humans. Additionally, their computational approach could be applied to other examples of convergent evolution where genomic data is available, allowing scientists to better understand how the same traits evolve in different species.

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© 2022, Kowalczyk et al.

Déclaration de conflit d'intérêts

AK, MC, NC No competing interests declared