Platypus and echidna genomes reveal mammalian biology and evolution

Abstract

Egg-laying mammals (monotremes) are the only extant mammalian outgroup to therians (marsupial and eutherian animals) and provide key insights into mammalian evolution1,2. Here we generate and analyse reference genomes of the platypus (Ornithorhynchus anatinus) and echidna (Tachyglossus aculeatus), which represent the only two extant monotreme lineages. The nearly complete platypus genome assembly has anchored almost the entire genome onto chromosomes, markedly improving the genome continuity and gene annotation. Together with our echidna sequence, the genomes of the two species allow us to detect the ancestral and lineage-specific genomic changes that shape both monotreme and mammalian evolution. We provide evidence that the monotreme sex chromosome complex originated from an ancestral chromosome ring configuration. The formation of such a unique chromosome complex may have been facilitated by the unusually extensive interactions between the multi-X and multi-Y chromosomes that are shared by the autosomal homologues in humans. Further comparative genomic analyses unravel marked differences between monotremes and therians in haptoglobin genes, lactation genes and chemosensory receptor genes for smell and taste that underlie the ecological adaptation of monotremes.

Towards complete and error-free genome assemblies of all vertebrate species

“…We successfully assembled both sex chromosomes (Z, W) for all three avian species, the first W chromosome (to our knowledge) for vocal learning birds (Extended Data Figs. 7, 9b), the X and/or Y chromosome in placental mammals (Canada lynx and two bat species), the X chromosome in the thorny skate, and for the first time, to our knowledge, all ten sex chromosomes (5X and 5Y) in the platypus 26 (Extended Data Fig. 9c).…”

“…Furthermore, we identified seven additional chromosomes (chromosomes [30][31][32][33][34][35][36] in the zebra finch, and eight (chromosomes 8, 9, 14, 15, 17, 19, 21, and X4; Extended Data Fig. 8a, b) in the platypus 26,27 . Relative to the VGP assembly, the earlier short-read Anna's hummingbird assembly was highly fragmented (Extended Data Fig.…”

“…oxytocin ligand and receptor gene families 57 ; 2) greater understanding of the evolution of the carbohydrate 6-O sulfotransferase gene family, which encodes enzymes that modify secreted carbohydrates 58 ; 3) the first Bat1K study 50 , which generated a genome-scale phylogeny that better resolves the relationships between bats and other mammals, and which identified changes in bat genes that are involved in immunity and life span, including genes that are relevant to the COVID-19 pandemic 59 ; 4) deleterious mutations that have been purged from the last surviving isolated and inbred population of the critically endangered kākāpō 60 ; and 5) more complete resolution of the evolution of the complex sex chromosomes in platypus and echidna 26 . These discoveries were not possible with the previous reference assemblies, and we expect many future discoveries to follow.…”

False gene and chromosome losses affected by assembly and sequence errors

“…In the previous platypus assembly, chromosomes were assigned, but the VGP assembly newly assigned six chromosomes (Chrs 8, 9, 16, 19, 21, and X4) containing 2,834 genes in total. Although much of these sequences were previously assembled, they were too short in size to be scaffolded into chromosomes 6,20 . In the previous climbing perch assembly, chromosomes were not assigned, and sequence continuity was also too short.…”

Evolutionary dynamics of the human pseudoautosomal regions

“…In eutherian mammals, with only few exceptions [1,2], genetic determination of sex is based on a chromosomal heteromorphism of the XX/XY type, in which males are heterogametic [3,4]. A mutation in a gene that would become a sex-determining master is thought to be responsible for triggering an evolutionary process of stepwise loss of recombination between the ancestral autosome pair [3,5,6].…”