Large-Scale Chromosomal Changes Lead to Genome-Level Expression Alterations, Environmental Adaptation, and Speciation in the Gayal (Bos frontalis)

Abstract

Determining the functional consequences of karyotypic changes is invariably challenging because evolution has a tendency to obscure many of its own footprints, such as accumulated mutations, recombination events and demographic perturbations. Here we describe the assembly of a chromosome-level reference genome of the gayal (Bos frontalis) thereby revealing the structure, at base-pair level resolution, of a telo/acrocentric-to-telo/acrocentric Robertsonian translocation (2; 28) (T/A-to-T/A rob(2; 28)). The absence of any reduction in the recombination rate or genetic introgression within the fusion region of gayal served to challenge the long-standing view of a role for fusion-induced meiotic dysfunction in speciation. The disproportionate increase noted in the distant interactions across pro-chr2 and pro-chr28, and the change in open-chromatin accessibility following rob(2; 28), may however have led to the various gene expression irregularities observed in the gayal. Indeed, we found that many muscle-related genes, located syntenically on pro-chr2 and pro-chr28, exhibited significant changes in expression. This, combined with genome-scale structural variants and expression alterations in genes involved in myofibril composition, may have driven the rapid sarcomere adaptation of gayal to its rugged mountain habitat. Our findings not only suggest that large-scale chromosomal changes can lead to alterations in genome-level expression, thereby promoting both adaptation and speciation, but also illuminate novel avenues for studying the relationship between karyotype evolution and speciation.

When Livestock Genomes Meet Third-Generation Sequencing Technology: From Opportunities to Applications

“…Following the advent of NGS, the de novo sequencing of livestock species became feasible, typically by constructing a reference genome based on a representative breed [13]. TGS technologies demonstrate remarkable advantages and enormous potential in genome assembly research, and they are widely applied in various animals, such as cattle [14,15], gayals [16], yaks [17,18], buffalos [19,20], sheep [21,22], goats [23,24], pigs [25,26], chickens [27,28], ducks [29], and geese [30] (Table 1).…”

Research Progress and Applications of Bovine Genome in the Tribe Bovini

“…In gayal, Chen et al [24] identified expanded gene families (e.g., MYH, DHPR, ROCK), a positive selection gene (MLCK2), segmental duplication, and core drive genes (e.g., RYR2, TNNI3, and ACTC1) based on the comparative genome and transcriptome analyses, mainly related to odor sensation and cardiac function (Table 3). Li et al [36] detected several differentially expressed genes on the newly derived chromosome 2, which is functionally shown to be strongly associated with muscle traits in gayal, an adaptation to the alpine valley they inhabit.…”

Structural Variants and Speciation: Multiple Processes at Play

“…While direct evidence remains scarce, testing this hypothesis is now possible with the emergence of new techniques (Hi-C, ATACseq) which may unveil additional mechanisms by which SV contribute to speciation (see e.g. Li et al 2023). A) The interchromosomal effect, i.e.…”