Evolution of B Chromosomes: From Dispensable Parasitic Chromosomes to Essential Genomic Players

Abstract

B chromosomes represent additional chromosomes found in many eukaryotic organisms. Their origin is not completely understood but recent genomic studies suggest that they mostly arise through rearrangements and duplications from standard chromosomes. They can occur in single or multiple copies in a cell and are usually present only in a subset of individuals in the population. Because B chromosomes frequently show unstable inheritance, their maintenance in a population is often associated with meiotic drive or other mechanisms that increase the probability of their transmission to the next generation. For all these reasons, B chromosomes have been commonly considered to be nonessential, selfish, parasitic elements. Although it was originally believed that B chromosomes had little or no effect on an organism’s biology and fitness, a growing number of studies have shown that B chromosomes can play a significant role in processes such as sex determination, pathogenicity and resistance to pathogens. In some cases, B chromosomes became an essential part of the genome, turning into new sex chromosomes or germline-restricted chromosomes with important roles in the organism’s fertility. Here, we review such cases of “cellular domestication” of B chromosomes and show that B chromosomes can be important genomic players with significant evolutionary impact.

Mendelian nightmares: the germline-restricted chromosome of songbirds

“…Some B chromosomes show meiotic drive increasing the chance of their transmission to the germ cells, while others, for example, show mitotic drive leading to the preferential segregation of both B chromosome chromatids to the germline (gonotaxis). Similarities between B chromosomes and GRCs have been previously noted (Johnson Pokorná and Reifová 2021 ) and it seems plausible that the latter might be a way of long-term stabilization of a B chromosome, i.e., a GRC would be a B chromosome with stable germline inheritance and somatic elimination. Such a B-chromosomal origin would be consistent with the female bias in GRC inheritance, akin to meiotic drive of B chromosomes often through the asymmetry of female meiosis (Jones 2018 ; Clark and Kocher 2019 ).…”

“…B chromosomes are supernumerary dispensable chromosomes, which occur in a single or multiple copies in the cell and often show unstable meiotic and mitotic inheritance, which may result in their loss from the population. Because they usually do not provide any advantage to their carriers (but see Johnson Pokorná and Reifová 2021 for exceptions) and can be even harmful especially if they occur in odd copy numbers (Camacho et al 2004 ), many B chromosomes evolved mechanisms to increase probability of their inheritance in a selfish way (Jones 2018 ). Some B chromosomes show meiotic drive increasing the chance of their transmission to the germ cells, while others, for example, show mitotic drive leading to the preferential segregation of both B chromosome chromatids to the germline (gonotaxis).…”

“…In most animals, the mitochondrial DNA is inherited only through females, although there are exceptions where mitochondrial DNA shows paternal or doubly uniparental inheritance (Sutherland et al 1998 ; Zouros 2013 ; Dégletagne et al 2021 ). Other more particular cases comprise the non-random segregation of B-chromosomes, sex chromosomes, centromeres, and various chromosome rearrangements via meiotic drive, which have been observed in many eukaryotes (De Villena and Sapienza 2001a , b ; Camacho 2005 ; Rutkowska and Badyaev 2008 ; Yoshida and Kitano 2012 ; Houben 2017 ; Johnson Pokorná and Reifová 2021 ). In some organisms, sex chromosomes, sets of chromosomes, or even one of the parental genomes is eliminated during early embryogenesis, deviating from standard Mendelian inheritance (Sánchez 2014 ; Dedukh and Krasikova 2022 ).…”

“…In contrast to the essential A chromosomes, which comprise autosomes and sex chromosomes, B chromosomes are supernumerary and dispensable (Randolph 1928 ). B chromosomes are known to be present in only a subset of individuals within a species (or even only a subset of cells within an individual) and often accumulated via non-Mendelian mechanisms (reviewed in Johnson Pokorná and Reifová 2021 ). The GRC resembles a mitotically unstable B chromosome as it is present in only a subset of cells within an individual and because individuals can differ in the number of GRC they carry (Pigozzi and Solari 1998 , 2005 ).…”

Individual Genetic Heterogeneity

“…Some DNA molecules have catalytic deoxyribozyme activities and can catalyze sequence-specific DNA depurination [ 198 ]. Various genetic components can act as reservoir of genetic material [ 199 , 200 ].…”