Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

Abstract

The abundance and composition of heterochromatin changes rapidly between species and contributes to hybrid incompatibility and reproductive isolation. Heterochromatin differences may also destabilize chromosome segregation and cause meiotic drive, the non-Mendelian segregation of homologous chromosomes. Here we use a range of genetic and cytological assays to examine the meiotic properties of a Drosophila simulans chromosome 4 (sim-IV) introgressed into D. melanogaster. These two species differ by 12-13% at synonymous sites and several genes essential for chromosome segregation have experienced recurrent adaptive evolution since their divergence. Furthermore, their chromosome 4s are visibly different due to heterochromatin divergence, including in the AATAT pericentromeric satellite DNA. We find a visible imbalance in the positioning of the two chromosome 4s in sim-IV/mel-IV heterozygote and also replicate this finding with a D. melanogaster 4 containing a heterochromatic deletion. These results demonstrate that heterochromatin abundance can have a visible effect on chromosome positioning during meiosis. Despite this effect, however, we find that sim-IV segregates normally in both diplo and triplo 4 D. melanogaster females and does not experience elevated nondisjunction. We conclude that segregation abnormalities and a high level of meiotic drive are not inevitable byproducts of extensive heterochromatin divergence. Animal chromosomes typically contain large amounts of noncoding repetitive DNA that nevertheless varies widely between species. This variation may potentially induce non-Mendelian transmission of chromosomes. We have examined the meiotic properties and transmission of a highly diverged chromosome 4 from a foreign species within the fruitfly Drosophila melanogaster. This chromosome has substantially less of a simple sequence repeat than does D. melanogaster 4, and we find that this difference results in altered positioning when chromosomes align during meiosis. Yet this foreign chromosome segregates at normal frequencies, demonstrating that chromosome segregation can be robust to major differences in repetitive DNA abundance.H ETEROCHROMATIC repeats at and near telomeres and centromeres turn over rapidly at short evolutionary time scales (Charlesworth et al. 1994). A subset of genes involved in meiosis, chromosome and chromatin function, and transposable element defense also show high rates of divergence between sibling species, often with accompanying signatures of adaptive evolution Begun et al. 2007;Larracuente et al. 2008;Anderson et al. 2009;Obbard et al. 2009;Raffa et al. 2011;Langley et al. 2012). These patterns suggest that organisms need to mount a continual adaptive response to suppress deleterious consequences caused by heterochromatic repetitive DNAs. Satellite DNAs and transposable elements, the major components of heterochromatin, can increase their copy numbers by unequal crossing over and transposition. These expansions can reduce fitness by increasing genome size and rates of...

Karyotype evolution in apomictic Boechera and the origin of the aberrant chromosomes

“…Despite the difference in the amount of heterochromatin between the Het and its (BS1/BD1) homologue, both chromosomes exhibit a regular bivalent pairing during meiosis I (Kantama et al ., ; Figure a). This observation is concordant with the observed regular meiotic pairing and segregation of heterochromatin divergent homeologues in Drosophila (Gilliland et al ., ). The Het chromosome is derived from B. stricta as based on hybridization of pericentromeric repeats (Schranz et al ., ; Kantama et al ., ).…”

Centromere-associated meiotic drive and female fitness variation inMimulus

“…; but see Gilliland et al. ). Thus, under a model in which all costs of female meiotic drive are pleiotropic effects of divergence in centromeric heterochromatin, recessive female costs are not predicted.…”

“…Because all products of male meiosis become gametes (gametophytes in plants), deleterious duplications and deletions of chromosomes caused by nondisjunction should be most evident in males. Furthermore, elevated rates of chromosomal nondisjunction in hybrids between taxa divergent in heterochromatin have been observed (McKee et al 1998; but see Gilliland et al 2015). Thus, under a model in which all costs of female meiotic drive are pleiotropic effects of divergence in centromeric heterochromatin, recessive female costs are not predicted.…”

Comparative Cytology of Female Meiosis I AmongDrosophilaSpecies

“…Because more published data were available for inversions than heterochromatin content, we selected some species that did not yet have their heterochromatin characterized, reasoning that they could be characterized later if the pattern looked promising. The D. melanogaster and D. simulans stocks had been maintained in our lab since the previous study (Gilliland, Colwell, Osiecki, et al 2015) while stocks of the new species were obtained from the Drosophila Species Stock Center at UC San Diego (now located at Cornell University), except for D. virilis which was a gift from Dr. Justin Blumenstiel (KU Lawrence) (see Table S1 for strain identifiers).…”

“…A recent study published in GENETICS (Gilliland, Colwell, Osiecki, et al 2015) melanogaster genetic background. While males homozygous for the foreign chromosome were sterile, homozygous females were fertile, and the introgressed chromosome still segregated accurately, both when homozygous as well as when heterozygous with a D. melanogaster chromosome 4.…”