Microchromosomes are building blocks of bird, reptile, and mammal chromosomes

Abstract

Microchromosomes, once considered unimportant shreds of the chicken genome, are gene-rich elements with a high GC content and few transposable elements. Their origin has been debated for decades. We used cytological and whole-genome sequence comparisons, and chromosome conformation capture, to trace their origin and fate in genomes of reptiles, birds, and mammals. We find that microchromosomes as well as macrochromosomes are highly conserved across birds and share synteny with single small chromosomes of the chordate amphioxus, attesting to their origin as elements of an ancient animal genome. Turtles and squamates (snakes and lizards) share different subsets of ancestral microchromosomes, having independently lost microchromosomes by fusion with other microchromosomes or macrochromosomes. Patterns of fusions were quite different in different lineages. Cytological observations show that microchromosomes in all lineages are spatially separated into a central compartment at interphase and during mitosis and meiosis. This reflects higher interaction between microchromosomes than with macrochromosomes, as observed by chromosome conformation capture, and suggests some functional coherence. In highly rearranged genomes fused microchromosomes retain most ancestral characteristics, but these may erode over evolutionary time; surprisingly, de novo microchromosomes have rapidly adopted high interaction. Some chromosomes of early-branching monotreme mammals align to several bird microchromosomes, suggesting multiple microchromosome fusions in a mammalian ancestor. Subsequently, multiple rearrangements fueled the extraordinary karyotypic diversity of therian mammals. Thus, microchromosomes, far from being aberrant genetic elements, represent fundamental building blocks of amniote chromosomes, and it is mammals, rather than reptiles and birds, that are atypical.

Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

“…The high global stability of macro- and microchromosomes between sea turtle families also aligns with recent work showing similar patterns across reptiles, including birds, emphasizing the important roles of microchromosomes in vertebrate evolution (55). Higher evolutionary rates for microchromosomes relative to macrochromosomes has been documented in intraspecific (56) and interspecific (57) studies with chicken and turkey genomes, respectively, so it is possible that the characteristics of microchromosomes and RRCs we observed are not unique to sea turtles, but rather, are prevalent in many vertebrates, which will become clearer as more high-quality assemblies are produced.…”

A paternal bias in germline mutation is widespread in amniotes and can arise independently of cell divisions

“…The genome of birds and snakes are organized into two types of autosomes, macro- and microchromosomes, which differ in their length, gene content, density of hypomethylated CpG islands, recombination rates and replication timing [82]. Given the idiosyncrasies of microchromosomes, which may affect the substitution rate estimates [60], we excluded sequences aligned to microchromosomes in birds and snakes (chromosomes 10 to 28 in Gallus gallus and chromosomes 13 to 18 in Crotalus viridis ).…”

Strategies for meiotic sex chromosome dynamics and telomeric elongation in Marsupials

“…Mammals (represented by monotremes, marsupials and eutherians) last shared a common ancestor approximately 185 million years ago (Mya) [4] and are characterised by distinctive genome plasticity [5,6]. Despite genome reshuffling, canonical features of the meiotic programme are well conserved in eutherian mammals (i.e., human, non-human primates, rodents and bovids) [3,[7][8][9][10][11][12].…”