Academic journal article Genetics

Stable Inheritance of Host Species-Derived Microchromosomes in the Gynogenetic Fish Poecilia Formosa

Academic journal article Genetics

Stable Inheritance of Host Species-Derived Microchromosomes in the Gynogenetic Fish Poecilia Formosa

Article excerpt

ABSTRACT

B chromosomes are additional, usually unstable constituents of the genome of many organisms. Their origin, however, is often unclear and their evolutionary relevance is not well understood. They may range from being deleterious to neutral or even beneficial. We have followed the genetic fate of B chromosomes in the asexual, all-female fish Poecilia formosa over eight generations. In this species, B chromosomes come in the form of one to three tiny microchromosomes derived from males of the host species that serve as sperm donors for this gynogenetic species. All microchromosomes have centromeric heterochromatin but usually only one has a telomere. Such microchromosomes are stably inherited, while the telomereless are prone to be lost in both the soma and germline. In some cases the stable microchromosome carries a functional gene lending support to the hypothesis that the B chromosomes in P. formosa could increase the genetic diversity of the clonal lineage in this ameiotic organism and to some degree counteract the genomic decay that is supposed to be connected with the lack of recombination.

B chromosomes are supernumerary chromosomes, which do not follow Mendelian rules of inheritance. To date, they have been found in >2000 species of plants, animals, and fungi (JONES and REES 1982; CAMACHO et al. 2000; PALESTIS et al. 2004). B chromosomes are considered either to arise from a duplicated or fragmented A chromosome within the same genome or to be acquired during a hybridization event from foreign DNA that evolves into the supernumerary chromosome (JONES and REES 1982; GREEN 1990; CAMACHO et al. 2000). Within a given species or population, individuals are polymorphic for the presence of B chromosomes, because the chromosomes usually lack a homologous partner to pair with during meiosis and are therefore distributed unequally to the gametes. There can be one or several B chromosomes in one individual. In addition B chromosomes can also be lost during an individual's development because of unequal distribution during cell divisions. Such organisms then may lack B chromosomes in certain organs, tissues, or cells (PALESTIS et al. 2004).

The maintenance and evolution of B chromosomes have been explained in several ways. Traditionally, they have been classified as selfish genetic elements that decrease the fitness of the "host" genome (SHAW and HEWITT 1990; CAMACHO et al. 2000). Thus they generate what has been called a "genetic conflict" between the A and B chromosomes. By virtue of their accumulation mechanisms, they are maintained within populations (ÖSTERGREN 1945; THOMSON 1984; JONES 1985; NUR et al. 1988). In the heterotic model (WHITE 1973), it is assumed that B chromosomes are maintained because they increase the fitness of the host when they occur at low frequency. This hypothesis does not require an accumulation mechanism. An "evolutionary arms race" model (CAMACHO et al. 1997) assumes a nonstable, dynamic situation. B chromosomes are considered parasitic and spread through the population because of an accumulation mechanism. But, as they increase their frequency, they are neutralized by the host genome and begin to disappear slowly, unless a new variant of the B, which can counteract the elimination mechanism, replaces the neutralized B.

Only in very few cases do the B chromosomes appear to have a beneficial effect on the host species (BOUGOURD and JONES 1997), while most are considered to be harmful (PALESTIS et al. 2004). They can, however, escape extinction in outcrossing species because they can continually "infect" new lineages if they drive. In inbred or asexual species, natural selection acts among competing lines of descendants or clones, respectively. Lines or clones without B chromosomes are expected to outcompete those with B chromosomes, if B chromosomes decrease fitness. In the asexual all-female fish species Poecilia formosa, the Amazon molly, supernumerary chromosomes have frequently been found in both laboratory-reared and wild-caught individuals from the Río Purificación/Río Soto la Marina river system, Mexico (LAMATSCH et al. …

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