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Pubertal Growth Spurt? Geckos Tell a Different Tale.

In humans, puberty is associated with a rapid growth spurt that underlies the many phenomena—such as voice cracking—that people commonly think of when the words ‘puberty’ and ‘maturation’ crop up. However, in vertebrates in general, growth and puberty/maturation are not always closely linked. One could argue that it is self-evident, given that, let’s say, reptiles grow their whole life and thus cannot be expected to reach their final body size when they become sexually mature. The issue is, a team of researchers from our faculty discovered a few years ago that reptiles in fact do not display indeterminate growth. Now another team of researchers, Brandon Meter and Zuzana Starostová from the Department of Zoology, Faculty of Science, and Lukáš Kratochvíl and Lukáš Kubička from the Department of Ecology, Faculty of Science, further delved into the mysteries of reptile growth. Their analysis of proximate causes of sexual size dimorphism in the Madagascar ground gecko (Paroedura picta) was recently published in Frontiers in Physiology.

Animals may display two basic modes of growth—determinate and indeterminate. Among vertebrates, the growth of mammals and birds is determinate. On the other hand, reptiles (excluding birds) were thought to be indeterminate growers who grow slowly, but their growth does not cease when they reach sexual maturity. Petra Frýdlová and her colleagues from our faculty have recently disputed this paradigm and demonstrated that reptiles also reach a final body size, though it happens long after sexual maturity is attained. This discovery has important implications for research of other aspects of reptile body size, e.g., now it is clear that it is important to control for whether or not a reptile has already stopped growing to prevent unnecessary artifacts. However, the research of reptile growth still poses many challenges. If we want to study a mammal that has already attained its final body size, we simply need to look at an adult individual. Reptiles with their determinate growth that continues long after maturity do not allow for an easy determination of when an individual reached its final body size.

None of this deterred the authors of the study focused on sexual dimorphism in Madagascar ground geckos (Paroedura picta). Sexual dimorphism occurs when two sexes of the same species markedly differ in their body shape, colouration, or body size. Sexual size dimorphism (SSD) is what occurs in the studied gecko as well as many other reptiles. Males are the larger sex in P. picta, most likely utilising their increased body size in territorial fights. However, what is the proximate cause of the size difference between males and females?

Madagascar ground gecko (Paroedura picta), source: Wikimedia, author: Charles J. Sharp

In the case of species with genetic sex differentiation, it would make sense to turn to sex-linked genes for answers. The issue is, SSD also occurs in animals with environmental sex determination and in sequential hermaphrodites. That is individuals who are both male and female, but not simultaneously. This occurs for example in clownfishes of the genus Amphiprion. These fish, which you may know as the protagonists of Finding Nemo, start their life as males, though given the right conditions, they may gain weight and transform into a female. Furthermore, SSD is caused by genes that are not sex-linked even in vertebrates where genetic sex determination does occur. So how can we identify the cause of SSD?

Thanks to an abundance of data from various vertebrates, it is possible to identify candidate genes (and their products) responsible for SSD. Moreover, it is known that SSD is not apparent from the hatching and appears only later in life. SSD should thus be caused by some factor which would occur in the body with greater intensity around the time the growth trajectories of the two sexes start to diverge. In the larger sex—in males of P. picta—should this unknown factor result in increased activity of growth plates. By the time the growth ceases should the levels of this factor decrease or at least lose their effect on the growth plates.

This is the basic framework of the gecko experiment. The authors studied individuals of both sexes till the animals were ca 22 months of age (when body growth ceases or is negligible) and monitored their growth, growth plate activity, size of gonads, and levels of sex hormones. Furthermore, they’ve also studied the expression of six candidate genes in selected age groups. Gene expression is basically indicating how active the gene’s transcription is, i.e., how much RNA it produces. The amount of transcribed RNA can then be compared between sexes in different age groups. If the aforementioned framework is correct, then around the time SSD appears, a change in the expression of genes involved in the dimorphic growth is expected. One of the six candidate genes indeed showed an expression pattern consistent with the framework, with a noticeable peak in expression in males around the time SSD started to be apparent. This gene was IGF1 (insulin-like growth factor 1), the product of which is a hormone responsible for the regulation of growth acting downstream of growth hormone (GH) signalisation. IGF1 also plays an important role both in humans and mice where it affects postnatal bone growth and regulates the activity of growth plates. It is also known to affect the evolution of body size in dogs. Furthermore, a spike in IGF1 is closely associated with a pubertal growth spurt.

In male geckos, the increase in expression of IGF1 occurs long after the animal attains sexual maturity, and it also does not correlate with gonadal size or testosterone levels. Furthermore, SSD occurs even in castrated males. What may then be the reason behind the absence of a similarly strong expression of IGF1 in females? The answer seems to lie in their ovaries, as females with removed ovaries seemed to grow in a similar fashion to males. This is probably due to the inhibitory effects of estrogen on growth plates. The role of increased levels of estrogen or estrogen receptors in growth inhibition and SSD has been also demonstrated in other reptiles, mice as well as humans. 

The decoupling of the increase in IGF1 and sexual maturation—so closely connected in mammals—thus brings forth a plethora of questions concerning the evolution of growth and body size. Furthermore, it highlights the importance of using non-model organisms to gain a better understanding of the diversity of various patterns observed in nature. It remains to see whether the findings from P. picta apply to other reptiles as well. Furthermore, some other species of the genus Paroedura are monomorphic or display SSD with larger females, and it will be no doubt interesting to explore how their growth is regulated. 

Kateřina Bezányiová

Meter, B., Kratochvíl, L., Kubička, L., & Starostová, Z. (2022). Development of male-larger sexual size dimorphism in a lizard: IGF1 peak long after sexual maturity overlaps with pronounced growth in males. Frontiers in physiology, 1502.

Published: Nov 07, 2022 11:00 AM

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