Extensive variation in chromosome number and genome size in sexual and parthenogenetic species of the jumping-bristletail genus Machilis (Archaeognatha)

Abstract

Parthenogenesis in animals is often associated with polyploidy and restriction to extreme habitats or recently deglaciated areas. It has been hypothesized that benefits conferred by asexual reproduction and polyploidy are essential for colonizing these habitats. However, while evolutionary routes to parthenogenesis are manifold, study systems including polyploids are scarce in arthropods. The jumping-bristletail genus Machilis (Insecta: Archaeognatha) includes both sexual and parthenogenetic species, and recently, the occurrence of polyploidy has been postulated. Here, we applied flow cytometry, karyotyping, and mitochondrial DNA sequencing to three sexual and five putatively parthenogenetic Eastern-Alpine Machilis species to investigate whether (1) parthenogenesis originated once or multiply and (2) whether parthenogenesis is strictly associated with polyploidy. The mitochondrial phylogeny revealed that parthenogenesis evolved at least five times independently among Eastern-Alpine representatives of this genus. One parthenogenetic species was exclusively triploid, while a second consisted of both diploid and triploid populations. The three other parthenogenetic species and all sexual species were diploid. Our results thus indicate that polyploidy can co-occur with parthenogenesis, but that it was not mandatory for the emergence of parthenogenesis in Machilis. Overall, we found a weak negative correlation of monoploid genome size (Cx) and chromosome base number (x), and this connection is stronger among parthenogenetic species alone. Likewise, monoploid genome size decreased with elevation, and we therefore hypothesize that genome downsizing could have been crucial for the persistence of alpine Machilis species. Finally, we discuss the evolutionary consequences of intraspecific chromosomal rearrangements and the presence of B chromosomes. In doing so, we highlight the potential of Alpine Machilis species for research on chromosomal and genome-size alterations during speciation.

Keywords: Asexuality; chromosomal speciation; genome downsizing; parthenogenesis; polyploidy.

Figure 1

Geographic locations of all populations sampled in this study. White and black symbols correspond to sexual and parthenogenetic species, respectively. Whenever more than one species was found at a location, species-specific symbols are connected by lines with that location.

Figure 2

Bayesian phylogeny based on 222 mitochondrial CO1 sequences from 12 Eastern-Alpine Machilis species and Lepismachilis y-signata as out-group. All nodes supported by posterior probabilities higher than 0.95 are indicated by stars. Red branches highlight parthenogenetic species. Species included in the phylogeny but excluded from other analyses have gray branches. Mean relative genome size and chromosome number are given for all species and major intraspecific clades. Diploid and triploid chromosome numbers are indicated by circled and squared symbols, respectively. The number of individuals used to calculate average genome size values (N) is given to the right side of bars. Error bars indicate standard deviation (SD).

Figure 3

Geographic locations of sampled Machilis helleri populations with corresponding number of chromosomes and mean relative genome size (±SD). Below, a simplified drawing of the corresponding branch of the mitochondrial phylogeny is displayed. All nodes supported by posterior probabilities higher than 0.95 are indicated by stars.

Figure 4

Correlation between elevation and chromosome base number (A), elevation and monoploid genome size (B), and chromosome base number and monoploid genome size (C). Sexual populations are represented by black dots, parthenogenetic populations by gray circles. Regression lines and correlation coefficients including P-values are given for all populations together (black line), just sexual populations (black dotted line), and just parthenogenetic populations (gray dashed line).

Figure 5

Relative genome size plotted for 191 Machilis individuals for which chromosome number has been determined as well. Individual measurements are grouped according to species affiliation and, in M. ticinensis and M. tirolensis, split according to reproductive mode (sexual/parthenogenetic) and ploidy level (diploid/triploid), respectively. Dark and light gray backgrounds indicate sexual and parthenogenetic mode of reproduction, respectively. Diploid individuals are represented by filled circles and triploids by empty squares. Chromosome number is coded using the same colors as in Fig. 2. Within groups, random horizontal scatter was applied to individuals for better visualization.