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

Abstract

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 ...

Independent Evolution of Sex Chromosomes in Eublepharid Geckos, A Lineage with Environmental and Genotypic Sex Determination

“…The male-heterogametic sex chromosomes in the genus Coleonyx are partially homologous to GGA1, GGA6 and GGA11 (this study), the XX/XY sex chromosomes of the pygopodid geckos to GGA4q [ 22 ], the ZZ/ZW sex chromosomes of the sphaerodactylid genus Aristelliger to GGA2 [ 24 ] and the ZZ/ZW sex chromosomes of several species of the genus Paroedura to GGA4p and GGA15 [ 16 ]. The sex chromosomes are homologous to the GGAZ syntenic block, both in the phyllodactylid Phyllodactylus wirshingi [ 23 ] and the gekkonid Gekko hokouensis [ 54 ], two widely diverged species phylogenetically separated by lineages with other sex determination systems [ 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 ]. Therefore, it seems that the ancestors of these two species independently co-opted the same region for the role of sex chromosomes rather than that sex chromosomes were in these two lineages inherited from their common ancestor.…”

“…Despite the overall variability in sex determination in geckos, it seems that sex chromosomes in several gekkotan lineages are old and stable. The legless geckos from the family Pygopodidae demonstrate a long-term stability of sex chromosomes for 32–72 MY [ 22 ]. Several species of the genus Paroedura (family Gekkonidae) demonstrate homologous sex chromosomes for 60–92 MY, with a more recent turnover of an inner clade to a novel GSD system [ 16 ].…”

“…We used a qPCR method to compare the relative gene copy variation between the male and female genome described in detail in Rovatsos and co-authors [ 16 , 22 , 65 , 66 , 67 ], in order to validate the X-specificity of the genes revealed from the comparative coverage analysis ( Table S3 ). In similar approach as for the comparative genome coverage, the XY males have double copies of X-specific genes compared to the XX females.…”

“…In any case, geckos are an excellent group for testing general hypotheses on sex determination. Molecular cytogenetics and next generation sequencing methodologies (e.g., DNAseq, RNAseq, RADseq) allow us to gradually start resolving the puzzle of the gecko variability in sex determination [ 7 , 16 , 22 , 23 , 24 ], but data are still scarce in this old, highly diversified lineage encompassing over 2000 currently recognized species [ 25 ]. Up to now, the eyelid geckos (family Eublepharidae), the gecko group with phylogenetically important position among squamates, was largely neglected in the application of modern sequencing approaches for the study of sex determination.…”

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

“…However, other lineages such as the caenophidian and non-caenophidian snakes, the xantusiid lizard Xantusia henshawi, the pygopodid geckos and skinks [63][64][65][66]…”