Conserved sex chromosomes and karyotype evolution in monitor lizards (Varanidae)

Abstract

Despite their long history with the basal split dating back to the Eocene, all species of monitor lizards (family Varanidae) studied so far share the same chromosome number of 2n = 40. However, there are differences in the morphology of the macrochromosome pairs 5-8. Further, sex determination, which revealed ZZ/ZW sex microchromosomes, was studied only in a few varanid species and only with techniques that did not test their homology. The aim of this study was to (i) test if cryptic interchromosomal rearrangements of larger chromosomal blocks occurred during the karyotype evolution of this group, (ii) contribute to the reconstruction of the varanid ancestral karyotype, and (iii) test homology of sex chromosomes among varanids. We investigated these issues by hybridizing flow sorted chromosome paints from Varanus komodoensis to metaphases of nine species of monitor lizards. The results show that differences in the morphology of the chromosome pairs 5-8 can be attributed to intrachromosomal rearrangements, which led to transitions between acrocentric and metacentric chromosomes in both directions. We also documented the first case of spontaneous triploidy among varanids in Varanus albigularis. The triploid individual was fully grown, which demonstrates that polyploidization is compatible with life in this lineage. We found that the W chromosome differs between species in size and heterochromatin content. The varanid Z chromosome is clearly conserved in all the analyzed species. Varanids, in addition to iguanas, caenophidian snakes, and lacertid lizards, are another squamate group with highly conserved sex chromosomes over a long evolutionary time.

Fig. 1

Schematic representation of the results of the FISH experiments with Varanus komodoensis chromosome paints. Results of female individuals are shown only for those species in which both sexes were studied. Phylogenetic relationships follow Lin and Wiens (2017). In V. albigularis albigularis, the studied individual was likely an exceptional spontaneous triploid

Fig. 2

Giemsa stained karyotype (left) and C-banded metaphases (right) of analyzed species. The W chromosomes in female karyotype were identified by sequential C-banding. The Z chromosomes are not assigned due to their similarity to other microchromosomes. Scale bars = 10 µm

Fig. 2

Giemsa stained karyotype (left) and C-banded metaphases (right) of analyzed species. The W chromosomes in female karyotype were identified by sequential C-banding. The Z chromosomes are not assigned due to their similarity to other microchromosomes. Scale bars = 10 µm

Fig. 3

Fluorescence in situ hybridization of Varanus komodoensis chromosomes paints. Arrowheads point to hybridization signals. Numbers are not given to microchromosomes as pairs are not distinguishable from each other by morphology. Scale bars = 10 µm

Fig. 4

Ancestral state reconstruction of morphology of chromosome pairs 5–8 using maximum parsimony. The phylogenetic relationships follow Lin and Wiens (2017)