Study reveals conservation of male-linked genes after loss of males in stick insects

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Traits are often lost during evolution, either because they are no longer useful or because they are too costly to maintain. When this happens, it is generally believed that the genes underlying the trait will also degrade, making it difficult if not impossible for the trait to reappear. However, there are many examples in nature of once-lost traits reappearing in later lineages.

According to Giobbe Forni, a researcher at the University of Bologna, “Mapping the presence and absence of traits on a species tree suggests that some traits may have been lost in the lineages leading to extant species and then restored. Wings in stick insects considered to be one of the most iconic cases of this evolutionary process.”

This means that the genes underlying these traits can be preserved, in some cases for millions of years. Unfortunately, research on the molecular basis of such reemergence is scarce, leaving the underlying mechanisms responsible for such preservation open to speculation until now.

In a new study published in Genome Biology and EvolutionForni and his colleagues shed light on another complex feature that has been lost in some stick insects—male production.

Loss of the ability to produce males results in female-only populations, which reproduce by parthenogenesis, a form of asexual reproduction. The study reveals that genes that are highly connected in regulatory networks and involved in multiple biological processes can be maintained long after a trait is lost, providing a potential pathway for trait reappearance over long evolutionary time scales.

In the new study, Forni and his co-authors Barbara Mantovani, Alexander S. Mikheyev and Andrea Luchetti conducted a comparative analysis of three species of stick insects in the genus Bacillus. While populations of Bacillus grandii marettimi consist of males and females that reproduce sexually, Bacillus atticus includes populations of only females that reproduce by parthenogenesis.

A third species, Bacillus rossius, includes sexual and parthenogenetic populations. By studying the fates of genes involved in male reproduction in these three species, the authors sought to investigate the extent to which genes are conserved after trait loss and the possible mechanisms driving this conservation.

The researchers first identified gene networks whose expression was associated with male or female reproduction in the sexual species B. marettimi and then evaluated the same genes in B. atticus and B. rossius. Surprisingly, male-linked genes showed no signs of weakened selection or accelerated evolution compared to female-linked genes in parthenogenetic species. Moreover, the expression patterns of male-associated genes were partially conserved in both parthenogenetic species.

Digging deeper, the researchers found that genes in the female-linked networks were predominantly expressed in female reproductive tissues, while those in the male-linked networks were expressed in both male and female reproductive tissues, including sexual and parthenogenetic females. This suggests that male-linked genes may also play roles in female reproduction.

The involvement of a gene in multiple biological processes is known as pleiotropy, and this phenomenon may explain the conservation of male-related genes in these parthenogenetic stick insects, as previously hypothesized.

Additionally, the authors found that genes that were highly connected to many other genes in the network were more likely to be expressed in the reproductive tissues of parthenogens, suggesting that a gene’s network connectivity may also influence gene conservation. his after the loss of features.

Taken together, these findings indicate “that the molecular ground plan of the once-lost male reproductive process may persist due to pleiotropic effects on other traits,” explains Forni. “Different genes may undertake different trajectories of conservation and decay depending on the level of pleiotropy within the gene regulatory network.”

This study not only sheds light on the persistence of genetic architecture after trait loss, but also provides a possible insight into the emergence of rare males and cryptic sex (ie, episodic male generation and sexual reproduction), which are observed in an increasing number of lines. which were thought to have lost the ability to produce males long ago. This opens up potential new avenues for research, with implications that could reach far beyond stick insects.

“Seeing how widespread genetic conservation is after trait loss is on a larger scale remains essential. Although the Bacillus species complex provides a good framework to address these issues, it would be useful to analyze a complex the largest species where multiple transitions between reproductive strategies have occurred,” notes Forni.

“While it is often necessary to rely on model species to discover and unravel biological processes, it is even more important to test our hypotheses in a broader context. This will only be possible if we devote more effort to observation and analyzing the amazing diversity of organisms and their complex adaptations.”

More information:
Giobbe Forni et al, Parthenogenetic stick insects exhibit signatures of conservation in the molecular architecture of male reproduction, Genome Biology and Evolution (2024). DOI: 10.1093/gbe/evae073

Magazine Information:
Genome Biology and Evolution

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