Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits

Phylogeny and characteristics of ruminants Ruminants are a diverse group of mammals that includes families containing well-known taxa such as deer, cows, and goats. However, their evolutionary relationships have been contentious, as have the origins of their distinctive digestive systems and headgear, including antlers and horns (see the Perspective by Ker and Yang). To understand the relationships among ruminants, L. Chen et al. sequenced 44 species representing 6 families and performed a phylogenetic analysis. From this analysis, they were able to resolve the phylogeny of many genera and document incomplete lineage sorting among major clades. Interestingly, they found evidence for large population reductions among many taxa starting at approximately 100,000 years ago, coinciding with the migration of humans out of Africa. Examining the bony appendages on the head—the so-called headgear—Wang et al. describe specific evolutionary changes in the ruminants and identify selection on cancer-related genes that may function in antler development in deer. Finally, Lin et al. take a close look at the reindeer genome and identify the genetic basis of adaptations that allow reindeer to survive in the harsh conditions of the Arctic. Science, this issue p. eaav6202, p. eaav6335, p. eaav6312; see also p. 1130 Ruminant phylogeny is resolved with representative genomes. INTRODUCTION The ruminants are one of the most successful mammalian lineages, exhibiting extensive morphological and ecological diversity and containing several key livestock species, such as cattle, buffalo, yak, sheep, and goat. Ruminants have evolved several distinct characteristics such as a multichambered stomach, cranial appendages (headgear), specialized dentition, a highly cursorial locomotion, and a wide range of body size variations. Despite their biological prominence and value to human societies, the evolutionary history of ruminants has not been fully resolved, and the molecular mechanisms underlying their particular characteristics remains largely unknown. RATIONALE We seek to resolve the controversies in the ruminant phylogeny and reveal the genetic basis underpinning the evolutionary innovations in ruminants. Here, we report the newly sequenced genomes of 44 ruminant species, covering about half the genera and all six extant Ruminantia families. We included seven published ruminant genomes (five bovids and two cervids) to reconstruct the phylogenetic tree by using improved time calibrations. We also reconstructed the Pleistocene demographic histories of these ruminant species using whole-genome heterozygosity information. Together with transcriptomic data of 516 samples from 68 tissues of four species, we conducted comparative genomic analyses to reveal candidate genes and regulatory elements that might have contributed to the evolution of the distinct ruminant characteristics. RESULTS Using whole-genome orthologous sequences obtained from 51 ruminants, we have produced a new well-supported ruminant phylogenetic tree. The new tree resolves previous controversies over the deep branches of ruminant families, as well as the highly radiated Bovidae family. We estimated the emergence of crown Ruminantia to the late Oligocene (39.1 million to 32.3 million years ago) and that of Pecora to the Neocene (23.3 million to 20.8 million years ago). Investigations of demographic history revealed massive population decline events that occurred in most ruminant species, starting from ~100,000 to 50,000 years ago, which was temporally and spatially concurrent with the increased human activities on different continents during this period. We further identified many genomic changes that associate with important evolutionary innovations, such as the multichambered stomach, headgear, body size variation, cursorial locomotion, and dentition. CONCLUSION Our results demonstrate the power of using comparative phylogenomic approaches in resolving the deep branches of phylogeny that result from rapid radiations. The data and results presented in this study provide valuable resources and insights into the evolution of ruminant and mammalian biology. Phylogeny and trait evolution of ruminants. The phylogenic tree of ruminants is presented with the species within same families and subfamilies collapsed. The ruminants have many textbook examples of distinct traits. The four-chambered stomach with omasum chamber is a key innovation evolved in pecoran ruminants. Headgear keratinous sheath only appear in Bovidae and Antilocapridae lineages. Many ruminants have evolved high-crowned or hypsodont teethes. The Antilocapridae and two bovid lineages are among the mammals with highest cursorial locomotion ability. The ruminants are one of the most successful mammalian lineages, exhibiting morphological and habitat diversity and containing several key livestock species. To better understand their evolution, we generated and analyzed de novo assembled genomes of 44 ruminant species, representing all six Ruminantia families. We used these genomes to create a time-calibrated phylogeny to resolve topological controversies, overcoming the challenges of incomplete lineage sorting. Population dynamic analyses show that population declines commenced between 100,000 and 50,000 years ago, which is concomitant with expansion in human populations. We also reveal genes and regulatory elements that possibly contribute to the evolution of the digestive system, cranial appendages, immune system, metabolism, body size, cursorial locomotion, and dentition of the ruminants.