Sex or no sex: evolutionary adaptation occurs regardless

Abstract

All species continuously evolve to adapt to changing environments. The genetic variation that fosters such adaptation is caused by a plethora of mechanisms, including meiotic recombination that generates novel allelic combinations in the progeny of two parental lineages. However, a considerable number of eukaryotic species, including many fungi, do not have an apparent sexual cycle and are consequently thought to be limited in their evolutionary potential. As such organisms are expected to have reduced capability to eliminate deleterious mutations, they are often considered as evolutionary dead ends. However, inspired by recent reports we argue that such organisms can be as persistent as organisms with conventional sexual cycles through the use of other mechanisms, such as genomic rearrangements, to foster adaptation.

Keywords: adaptation; asexual; genome evolution; meiosis; mitosis; recombination.

Figure 1

Genomic rearrangements in the asexual fungus Verticillium dahliae. A: Pulsed-field gel electrophoresis shows karyotype variations between 11 V. dahliae strains (bold; strains used in genome alignment). B: Extensive genomic rearrangements between V. dahliae strains JR2 and VdLs17 revealed by whole-genome alignment of the sequenced genomes (forward-forward alignment, red; inversions, blue). Data modified from [11].

Figure 2

Mechanisms of eukaryotic genome evolution. Several mechanisms can alter the genetic material of eukaryotic species: A: DNA point mutations (stars) can alter single (or few) nucleotides. B: Genetic material can be transferred from a donor lineage over species barriers (dashed line) into the genome of an acceptor lineage. This can either be limited to single genes (horizontal gene transfer; HGT) or comprise entire chromosomes (horizontal chromosome transfer; HCT). C: Inter- or intra-chromosomal rearrangements can lead to a variety of genomic changes. Double-strand breaks (DSBs) are indicated by red arrows and dashed lines.

Figure 3

Double-strand break repair pathways. Spontaneous or Spo11-induced double-strand breaks (DSBs) are pre-processed by the MRX complex and repaired by various pathways. Non-homologous end joining (NHEJ) will ligate DSBs. After further processing by the nucleases Exo1 and binding of Rad51, several break repair pathways such as double-strand break repair (DSBR), the synthesis-dependent strand annealing (SDSA), break-induced replication (BIR) and Rad51-independent single-strand annealing (SSA) can operate on DSBs.

Figure 4

Genomic rearrangements create karyotype diversity. Genomic rearrangements alter the genetic makeup (different shades of cells indicate distinct genetic makeup) and differently foster evolution during sexual, unisexual, parasexual, and asexual reproduction. During sexual reproduction, two cells from opposite mating types (a and α) fuse. Meiotic recombination leads to novel combinations of alleles, and rearrangements can further increase genetic variation. During unisexual reproduction, two cells of the same mating type fuse and meiotic recombination may generate novel allelic combinations. During parasexual reproduction two cells, independent of their mating type, fuse which is occasionally followed by the fusion of nuclei. These fused nuclei are genetically unstable and undergo non-meiotic recombination and chromosomal loss. During asexual reproduction, genomic rearrangements during mitosis, facilitated by repetitive elements and horizontal gene transfer, can generate genetic variation.