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Amniotes possess variability in sex determining mechanisms, however, this diversity is still only partially known throughout the clade and sex determining systems still remain unknown even in such a popular and distinctive lineage as chameleons (Squamata: Acrodonta: Chamaeleonidae). Here, we present evidence for female heterogamety in this group. The Malagasy giant chameleon ( Furcifer oustaleti) (chromosome number 2n = 22) possesses heteromorphic Z and W sex chromosomes with heterochromatic W. The panther chameleon ( Furcifer pardalis) (2n = 22 in males, 21 in females), the second most popular chameleon species in the world pet trade, exhibits a rather rare Z 1Z 1Z 2Z 2/Z 1Z 2W system of multiple sex chromosomes, which most likely evolved from W-autosome fusion.
Notably, its neo-W chromosome is partially heterochromatic and its female-specific genetic content has expanded into the previously autosomal region. Showing clear evidence for genotypic sex determination in the panther chameleon, we resolve the long-standing question of whether or not environmental sex determination exists in this species. Together with recent findings in other reptile lineages, our work demonstrates that female heterogamety is widespread among amniotes, adding another important piece to the mosaic of knowledge on sex determination in amniotes needed to understand the evolution of this important trait.
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Chameleons (family Chamaeleonidae) are well-known, highly distinctive lizards characterised by their unique morphological and physiological traits, such as independently movable stereoscopic eyes, projectable, ballistic tongue, prehensile feet and the notable ability in many species to change the colour of their skin. Currently, 200 extant species are recognized, distributed in Africa, Madagascar, Southern Europe and Southern Asia.
For a lizard family, chameleons have a relatively recent origin, with the basal split dated at approximately 65 million years ago.Despite the popularity of chameleons among herpetologists, private breeders and hobbyists, their sex determination has remained largely unstudied. In general, reptiles show a wide diversity of sex determination systems, including female heterogamety, male hetorogamety and environmental, particularly temperature-dependent, sex determination. Chameleons are an interesting group for the study of the evolution of sex determination as their sister lineage, dragon lizards (Agamidae), possesses either female heterogamety or environmental sex determination, while the next outgroup, iguanas (Pleurodonta), are typified by male heterogamety and a high evolutionary stability of sex chromosomes. Although temperature-dependent sex determination has been anecdotally reported for several chameleon species, e.g., Furcifer pardalis, Chamaeleo chameleon, C. Calyptratus, the evidence for it is not supported by controlled experiments. Moreover, where such experiments were performed, they showed that hatchling sex ratios do not deviate significantly from 1:1 at different constant incubation temperatures in F. Pardalis, nor in C.
The observation of equal sex ratios across constant incubation temperatures led to the conclusion that chameleons possess genotypic sex determination.Surprisingly, chameleons are relatively poorly studied cytogenetically and karyotypes are known for only 50 out of about 200 extant species. They possess karyotypes with chromosomal numbers varying from 2n = 20 to 2n = 36 (ref.
However, all known karyotypes have only been studied using exclusively “classical” cytogenetic techniques and molecular cytogenetic approaches have not yet been applied. In addition, sex chromosomes have not been described in any species, largely as few of these studies examined both males and females, which precluded the discovery of sex chromosomes.
The only known exception has come from Gordon (pers. Reported in ref.
) who suggested the existence of a female heterogametic system in Bradypodion ventrale, in response to the observation of the different chromosomal number existing between males (2n = 34) and females (2n = 35). Unfortunately though, to our knowledge, neither karyotypes of this species, nor any other additional information which would enable the testing of sex-linkage of the polymorphism in chromosomal numbers, has been published.This lack of comprehensive data prompted us to apply both classical (Giemsa staining, C-banding) and molecular (comparative genomic hybridization CGH, fluorescence in situ hybridization FISH) cytogenetic approaches to reveal the karyotype and particularly the sex chromosomes of two species of chameleons from the genus Furcifer. The panther chameleon ( Furcifer pardalis) and Malagasy giant chameleon ( Furcifer oustaleti) are endemic to Madagascar and adjacent islands, with the panther chameleon also being recently introduced to Reunion Island and Mauritius and the Malagasy giant chameleon becoming established near Nairobi in Kenya. In Madagascar, both species are common in lowlands, occupying a variety of habitats, such as scrub and forest and have so far survived the increased levels of habitat exploitation and degradation caused by human activities. The chameleons of the genus Furcifer possess karyotypes with chromosomal numbers varying between 2n = 22 and 2n = 28 (ref. ) and karyotypes with 2n = 22 chromosomes were reported for both F.
Pardalis and F. Panther chameleons exhibit high variation in colouration with several geographically distinct colour morphs. In addition, due to their variegated colouration, relatively easy care and reproduction in captivity they are very popular pets in North America and Europe with large numbers being bred commercially. The 664 bp sequence corresponding to the 5′ end of the mitochondrial locus cytochrome c oxidase I (COI), was successfully amplified and sequenced in the studied chameleons.
The haplotype analysis of our dataset in DnaSP v5.10.1 revealed five haplotypes for F. Pardalis and two for F. Oustaleti, none of which previously reported in the GenBank. The pooled sequences of COI from both our work and those derived from the GenBank show that F.
Pardalis altogether demonstrates a low mean genetic variation of 1.5%, while F. Oustaleti show a relative high genetic variation of 5.9%.
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Pardalis, all 7 males share the karyotype of 2n = 22, however all 6 females possess 2n = 21. The linkage of different chromosomal numbers to sex is statistically highly significant (p = (1/2) = 0.00012) we studied 13 individuals and probability that it would be found in a given sex just by chance is ½, which supports the identification of the chromosomes differing between males and females as the sex chromosomes. In females, the q-arm of one chromosome of the third largest chromosomal pair (FPA3) is always longer than its counterpart and this larger chromosome is not present in the male karyotypes. This chromosome seems to be partially heterochromatic, based on C-banding and shows strong female-specific genetic content according to CGH. Moreover, there is a single small unpaired metacentric chromosome (FPA10) in the female karyotypes.
On the contrary, in males, the third largest pair of chromosomes (FPA3) is homomorphic and the FPA10 pair consists of two homomorphic, metacentric chromosomes. This situation corresponds to the Z 1Z 1Z 2Z 2/Z 1Z 2W sex determination system. As we did not notice any differences in karyotypes among individuals with different haplotypes and from separate regions/colour morphs, the differences between sexes in chromosome number and morphology cannot therefore be attributed to geographic variation in karyotype or to the hybridization of different karyotype races. The karyotype of both sexes of F. Oustaleti consists of 2n = 22. However, we noticed heteromorphy of the second smallest chromosomal pair (FOU10) in the female karyotype , while both chromosomes of FOU10 are of equal size and shape in males.
The larger, female-specific chromosome of FOU10 is strongly heterochromatic as visualized by C-banding and contains female-specific sequences as revealed by CGH. Although our sample size in F.
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Oustaleti is small, the similarity of karyotypes in both studied species, the heterochromatic content of the submetacentric chromosome and its distinctness in CGH enable us to conclude that the submetacentric chromosome FOU10 in females can be assigned as the W sex chromosome. In addition to the expected terminal topology, FISH with the probe specific for the telomeric motif revealed extended interstitial telomeric repeats (ITRs), in both species (e and e). Pardalis, telomeric-like sequences were detected in the centromeric regions of six chromosomal pairs (1, 4–8) and interstitial positions in three chromosomal pairs (1, 2, 4) and in the W chromosome. Oustaleti, telomeric-like sequences were detected in the centromeric regions of four chromosomal pairs (1–4) and in the pericentromeric and interstitial positions of eight chromosomal pairs (1–8).In both species, we identified a strong signal of the rRNA probe in the fourth largest chromosomal pair localized in the region of the secondary constriction (h and h). Our results provide the first unequivocal evidence of the presence of sex chromosomes in any species of chameleons. We can conclude that chameleons of the genus Furcifer possess female heterogamety with well-differentiated sex chromosomes.
In earlier studies, the differences in chromosome number between males and females in F. Pardalis were not noticed.
We think that the discrepancy can be attributed to the limitations of microscopy and chromosome preparation techniques at the time of the earlier studies (see also ref. For another recent correction of the original cytogenetic data).
In addition, neither the sex, nor the number of studied chameleon individuals were indicated and perhaps mainly male individuals were karyotyped and in several cases, testicular tissue was used for metaphase preparations, and thus, the authors of the earlier studies were not able to identify the neo-W chromosome. The previous unpublished record by Gordon (pers. Reported in ref.