Most cited article - PubMed ID 23393279
Neither male gonadal androgens nor female reproductive costs drive development of sexual size dimorphism in lizards
During meiotic prophase I, tightly regulated processes take place, from pairing and synapsis of homologous chromosomes to recombination, which are essential for the generation of genetically variable haploid gametes. These processes have canonical meiotic features conserved across different phylogenetic groups. However, the dynamics of meiotic prophase I in non-mammalian vertebrates are poorly known. Here, we compare four species from Sauropsida to understand the regulation of meiotic prophase I in reptiles: the Australian central bearded dragon (Pogona vitticeps), two geckos (Paroedura picta and Coleonyx variegatus) and the painted turtle (Chrysemys picta). We first performed a histological characterization of the spermatogenesis process in both the bearded dragon and the painted turtle. We then analyzed prophase I dynamics, including chromosome pairing, synapsis and the formation of double strand breaks (DSBs). We show that meiosis progression is highly conserved in reptiles with telomeres clustering forming the bouquet, which we propose promotes homologous pairing and synapsis, along with facilitating the early pairing of micro-chromosomes during prophase I (i.e., early zygotene). Moreover, we detected low levels of meiotic DSB formation in all taxa. Our results provide new insights into reptile meiosis.
- Keywords
- DSBs, bouquet, gametogenesis, meiosis, micro-chromosomes, recombination, reptile,
- Publication type
- Journal Article MeSH
Squamate reptiles have been considered to be indeterminate growers for a long time. However, recent studies demonstrate that bone prolongation is stopped in many lizards by the closure of bone growth plates. This shift in the paradigm of lizard growth has important consequences for questions concerning the proximate causes of sexual size dimorphism. The traditional model of highly plastic and indeterminate growth would correspond more to a long-term action of a sex-specific growth regulator. On the other hand, determinate growth would be more consistent with a regulator acting in a sex-specific manner on the activity of bone growth plates operating during the phase when a dimorphism in size develops. We followed the growth of males and females of the male-larger Madagascar ground gecko (Paroedura picta) and monitored the activity of bone growth plates, gonad size, levels of steroids, expression of their receptors (AR, ESR1), and expression of genes from the insulin-like growth factor network (IGF1, IGF2, IGF1R, and IGF2R) in livers. Specifically, we measured gene expression before the onset of dimorphic growth, at the time when males have more active bone growth plates and sexual size dimorphism was clearly visible, and after a period of pronounced growth in both sexes. We found a significant spike in the expression of IGF1 in males around the time when dimorphism develops. This overexpression in males comes long after an increase in circulating testosterone levels and sexual maturation in males, and it might be suppressed by ovarian hormones in females. The results suggest that sexual size dimorphism in male-larger lizards can be caused by a positive effect of high levels of IGF1 on bone growth. The peak in IGF1 resembles the situation during the pubertal growth spurt in humans, but in lizards, it seems to be sex-specific and disconnected from sexual maturation.
- Keywords
- IGF1, body size, bone, growth, hormones, reptiles, sexual size dimorphism, testosterone,
- Publication type
- Journal Article MeSH
(1) In contrast to mammals and birds, reptiles have been considered as indeterminate growers, whose growth reflects differential allocation of resources to growth versus other energetically demanding processes such as reproduction. (2) We monitored the growth and activity of bone growth plates, hormonal profiles, and reproductive activity in males and females of the male-larger gecko Paroedura picta. We show that growth plates fuse in this species in a sex-specific manner. The more abrupt epiphyseal closure and more pronounced growth deceleration in females coincide with the increased activity of their reproductive organs. (3) We conclude that at least some lizards are determinate growers whose sexual size dimorphism is potentially driven by ovarian hormones. The major difference in growth between endothermic and ectothermic amniotes appears to be in the magnitude of growth before and after the first reproduction, not in the mechanistic processes such as senescence of growth plate cells.
- Keywords
- Evolutionary biology, Evolutionary developmental biology, Ichthyology, Zoology,
- Publication type
- Journal Article MeSH
Proximate control of the development of sexual dimorphism is still hotly debated in reptiles. In some squamates, many male-typical exaggerated traits including body size were assumed to be controlled by masculinization by male gonadal androgens. We performed a manipulative experiment to test the importance of this mechanism in the development of pronounced sexual differences in body size and size of head casque in the chameleon Chamaeleo calyptratus. Castrated males attained male-typical body size highly deviating from the body size of control females. Ontogenetic allometries of casque size on head length revealed that sexes depart considerably in casque growth later in the ontogeny; however, castrated males still follow male-typical casque growth. Paradoxically, exogenous testosterone led in females to slight increase of casque size, which might reflect interference with the feminizing effects of female gonadal hormones. The results in males strongly suggest that masculinization by male gonadal androgens during growth is not required for the development of sexual dimorphism in body size and casque size in the chameleon. The ontogeny of sexually dimorphic body size and exaggerated traits in at least some squamates is likely controlled by other proximate mechanism, possibly by feminization by ovarian hormones.
- MeSH
- Androgens genetics metabolism MeSH
- Gonads metabolism MeSH
- Lizards anatomy & histology genetics growth & development metabolism MeSH
- Castration MeSH
- Skull anatomy & histology metabolism MeSH
- Sex Characteristics * MeSH
- Testosterone genetics metabolism MeSH
- Body Size genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Androgens MeSH
- Testosterone MeSH
An extensive research effort is devoted to the evolution of life-histories and processes underlying the variation in adult body weight; however, in this regard, some animal taxa remain neglected. Here we report rates and timing of growth recorded in two wild-derived populations of a model lizard species, Eublepharis macularius (M, W), other two related species, i.e., E. angramainyu (A) and E. sp. (D), and their between-species hybrids. We detected clear differences among the examined species/populations, which can be interpreted in the terms of "fast - slow" continuum of life-history strategies. The mean asymptotic body size was the highest in A and further decreased in the following order: M, W, and D. In contrast, the growth rate showed an opposite pattern. Counter-intuitively, the largest species exhibited the slowest growth rates. The final body size was determined mainly by the inflexion point. This parameter reflecting the duration of exponential growth increased with mean asymptotic body size and easily overcompensated the effect of decreasing growth rates in larger species. Compared to the parental species, the F1 and backcross hybrids exhibited intermediate values of growth parameters. Thus, except for the case of the F2 hybrid of MxA, we failed to detect deleterious effects of hybridization in these animals with temperature sex determination.
- MeSH
- Breeding MeSH
- Species Specificity MeSH
- Body-Weight Trajectory * MeSH
- Hybridization, Genetic genetics physiology MeSH
- Lizards growth & development MeSH
- Reproduction MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Comparative Study MeSH
Among amniote vertebrates, geckos represent a clade with exceptional variability in sex determination; however, only a minority of species of this highly diverse group has been studied in this respect. Here, we describe for the first time a female heterogamety in the genus Paroedura, the group radiated in Madagascar and adjacent islands. We identified homomorphic ZZ/ZW sex chromosomes with a highly heterochromatic W chromosome in Paroedura masobe, Paroedura oviceps, Paroedura karstophila, Paroedura stumpffi, and Paroedura lohatsara. Comparative genomic hybridization (CGH) revealed that female-specific sequences are greatly amplified in the W chromosome of P. lohatsara and that P. gracilis seems to possess a derived system of multiple sex chromosomes. Contrastingly, neither CGH nor heterochromatin visualization revealed differentiated sex chromosomes in the members of the Paroedura picta-Paroedura bastardi-Paroedura ibityensis clade, which is phylogenetically nested within lineages with a heterochromatic W chromosome. As a sex ratio consistent with genotypic sex determination has been reported in P. picta, it appears that the members of the P. picta-P. bastardi-P. ibityensis clade possess homomorphic, poorly differentiated sex chromosomes and may represent a rare example of evolutionary loss of highly differentiated sex chromosomes. Fluorescent in situ hybridization (FISH) with a telomeric probe revealed a telomere-typical pattern in all species and an accumulation of telomeric sequences in the centromeric region of autosomes in P. stumpffi and P. bastardi. Our study adds important information for the greater understanding of the variability and evolution of sex determination in geckos and demonstrates how the geckos of the genus Paroedura provide an interesting model for studying the evolution of the sex chromosomes.
- MeSH
- Biological Evolution * MeSH
- Phylogeny MeSH
- Heterochromatin genetics MeSH
- In Situ Hybridization, Fluorescence MeSH
- Lizards genetics MeSH
- Karyotyping MeSH
- Sex Chromosomes genetics MeSH
- Sex Determination Processes genetics MeSH
- Comparative Genomic Hybridization MeSH
- Telomere genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Heterochromatin MeSH