Escaping the evolutionary trap? Sex chromosome turnover in basilisks and related lizards (Corytophanidae: Squamata)

Nielsen, Stuart V.; Guzmán-Méndez, Irán Andira; Gamble, Tony; Madison, Blumer,; Pinto, Brendan J; Kratochvíl, Lukáš; Rovatsos, Michail

doi:10.1098/rsbl.2019.0498

Cited by 40 publications

(50 citation statements)

References 45 publications

(73 reference statements)

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“…A higher degree of differentiation in lineages with female heterogamety in comparison to male heterogamety was observed within snakes [82], chameleons [36,37], and between closely related teiid and lacertid lizards (20,83). On the other hand, XX/XY sex chromosomes are highly differentiated in viviparous mammals and iguanas [with the exception of basilisks 76,84]; however, sex chromosomes in these two groups are among the oldest sex chromosomes uncovered to date in amniotes and have thus potentially had a longer time to differentiate [85,86]. Moreover, these two lineages are the only amniote lineages with a chromosome-wide dosage compensation mechanism [87][88][89], which might influence the rate of differentiation of sex chromosomes.…”

Section: Discussionmentioning

confidence: 92%

Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

Kostmann

Kratochvíl

Rovatsos

2020

Preprint

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Differentiated sex chromosomes are believed to be evolutionarily stable, and their emergence was suggested to lead to a remarkable increase in the diversification rate and in disparity in such groups as birds, mammals and snakes. On the other hand, poorly differentiated sex chromosomes are considered to be prone to turnovers. With around 1.700 currently known species forming c. 15% of reptile species diversity, skinks (family Scincidae) are a very diverse group of squamates known for their large ecological and morphological variability. Skinks generally have poorly differentiated and cytogenetically hardly distinguishable sex chromosomes and their sex determination was suggested to be highly variable. Here, we determined X-linked genes in the common sandfish (Scincus scincus) and demonstrate that skinks have shared the same homologous XX/XY sex chromosomes across their wide phylogenetic spectrum for at least 85 million years, approaching the age of the highly differentiated ZZ/ZW sex chromosomes of birds and advanced snakes. Skinks thus demonstrate that even poorly differentiated sex chromosomes can be evolutionarily stable and that large diversity can emerge even in groups with poorly differentiated sex chromosomes. The conservation of sex chromosomes across skinks allows us to introduce the first molecular sexing method widely applicable in this group.

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Section: Discussionmentioning

confidence: 92%

Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

Kostmann

Kratochvíl

Rovatsos

2020

Preprint

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“…Amniotes (mammals and sauropsids) evolved sex chromosomes independently around 40 times, with geckos representing about half of the recorded transitions 25,26 . Currently, we know genes linked to sex chromosomes in only 16 amniote lineages with putative independently evolved sex chromosomes (reviewed in 13,27 ) and gene dose regulatory mechanisms were studied in just eight of these lineages (Table 1). In our quest for understanding the evolution of sex determination and gene dose regulatory mechanisms, we focus here on the pygypodid geckos (family Pygopodidae).…”

Section: Introductionmentioning

confidence: 99%

Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos

Rovatsos

Gamble

Nielsen

et al. 2020

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19Differentiation of sex chromosomes is thought to have evolved with cessation of 20 recombination and subsequent loss of genes from the degenerated partner (Y and W) of sex 21 chromosomes, which in turn leads to imbalance of gene dosage between sexes. Based on 22 work with traditional model species, theory suggests that unequal gene copy numbers lead to 23 the evolution of mechanisms to counter this imbalance. Dosage compensation, or at least 24 achieving dosage balance in expression of sex-linked genes between sexes, has largely been 25 documented in lineages with male heterogamety (XX/XY sex determination), while ZZ/ZW 26 systems are assumed to be usually associated with the lack of chromosome-wide gene dose 27 regulatory mechanisms. Here we document that although the pygopodid geckos evolved male 28 heterogamety with a degenerated Y chromosome 32-72 million years ago, one species in 29 particular, Burton's legless lizard (Lialis burtonis), does not possess dosage balance in the 30 expression of genes in its X-specific region. We summarize studies on gene dose regulatory 31 mechanisms in animals and conclude that there is in them no significant dichotomy between 32 male and female heterogamety. We speculate that gene dose regulatory mechanisms are likely 33 to be related to the general mechanisms of sex determination instead of type of heterogamety. 34Differentiated sex chromosomes evolved independently in numerous animal and plant 36 lineages 1 . The differentiation is connected with cessation of recombination and subsequent 37 loss of functional genes from the Y or W sex chromosomes which leads to gene dose 38 differences between sexes. Selection will favour the evolution of mechanisms that regulate 39 these differences at the cellular level, as alterations in gene copy number generally alters gene 40 expression, ultimately impacting cell physiology and organismal fitness 2-5 . Different taxa 41 have evolved distinct strategies to regulate the unequal gene copy numbers and the associated 42 gene dosage imbalances between the sexes related to differentiated sex chromosomes 6 . The 43 most well-known mechanism is dosage compensation, which restores the expression of X or 44 Z-specific genes in the heterogametic sex to the ancestral expression levels 7-9 . Dosage 45 compensation usually leads to dosage balance, i.e. equal expression levels of the X or Z-46 specific genes between the sexes, however some animal lineages can reach dosage balance in 47 the expression between sexes without keeping the ancestral expression level. Other animal 48 lineages do not compensate and balance expression in the majority of the sex-linked genes at 49 either the level of transcription or translation 10,11 . Dosage compensation or at least dosage 50 balance between sexes was documented largely in lineages with male heterogamety (XX/XY 51 sex determination) such as in several insect lineages, nematode worms, the green anole and 52 eutherian mammals, with sticklebacks, basilisks and platypus being exceptions 6,12,13 . On the 53 ...

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“…Namely, the lineage examined by Srikulnath et al [2014] might have experienced a sex chromosome turnover, leading to the loss of the original lacertid sex chromosome system and appearance of a new system, based on another chromosome pair. The cases of such turnovers, when a taxon "forsakes" a well-established sex chromosome system and acquires a new one, are rather rare , but known in lizards [Nielsen et al, 2019] and even in mammals [Matveevsky et al, 2017]. An intraspecific polymorphism in sex-determining systems is also possible, as in the case of the frog Glandirana rugosa [Ogata et al, 2018].…”

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confidence: 99%

Chromosome Painting Does Not Support a Sex Chromosome Turnover in Lacerta agilis Linnaeus, 1758

Lisachov

Giovannotti

Pereira

et al. 2020

Cytogenet Genome Res

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Reptiles show a remarkable diversity of sex determination mechanisms and sex chromosome systems, derived from different autosomal pairs. The origin of the ZW sex chromosomes of Lacerta agilis, a widespread Eurasian lizard species, is a matter of discussion: is it a small macrochromosome from the 11-18 group common to all lacertids, or does this species have a unique ZW pair derived from the large chromosome 5? Using independent molecular cytogenetic methods, we investigated the karyotype of L. agilis exigua from Siberia, Russia, to identify the sex chromosomes. FISH with a flow-sorted chromosome painting probe derived from L. strigata and specific to chromosomes 13, 14, and Z confirmed that the Z chromosome of L. agilis is a small macrochromosome, the same as in L. strigata. FISH with the telomeric probe showed an extensive accumulation of the telomere-like repeat in the W chromosome in agreement with previous studies, excluding the possibility that the lineages of L. agilis studied in different works could have different sex chromosome systems due to a putative intra-species polymorphism. Our results reinforce the idea of the stability of the sex chromosomes and lack of evidence for sex-chromosome turnovers in known species of Lacertidae.

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Escaping the evolutionary trap? Sex chromosome turnover in basilisks and related lizards (Corytophanidae: Squamata)

Cited by 40 publications

References 45 publications

Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

Do male and female heterogamety really differ in expression regulation? Lack of global dosage balance in pygopodid geckos

Chromosome Painting Does Not Support a Sex Chromosome Turnover in Lacerta agilis Linnaeus, 1758

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