Study reveals retention of male-related genes after loss of males in stick insects

Traits are often lost during evolution, either because they are no longer beneficial or because they are too costly to maintain. When this happens, it is generally believed that the genes underlying the trait will also eventually become degraded, making it difficult or impossible for the trait to re-emerge. Yet there are many examples in nature of once-lost traits reappearing in descendant lines.

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 existing species and then reinstated. are considered one of the most emblematic examples of this evolutionary process.

This implies that the genes underlying these traits can be preserved, in some cases for millions of years. Unfortunately, research into the molecular basis of such re-emergence is rare, leaving the underlying mechanisms responsible for such preservation thus far largely open to speculation.

In a new study published in Genome biology and evolutionForni and his colleagues shed light on another complex trait that has been lost in some stick insects: male production.

Loss of the ability to produce males results in populations consisting only of females, 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 retained long after the loss of a trait, providing a potential pathway for the re-emergence of a trait over long scales of evolving times.

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

A third species, Bacillus rossius, includes both sexual and parthenogenetic populations. By studying the fate of genes involved in male reproduction in these three species, the authors sought to study the extent to which genes are preserved after the loss of traits and the potential mechanisms behind this preservation.

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

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

The involvement of a gene in multiple biological processes is known as pleiotropy, and this phenomenon may explain the preservation 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 its preservation. after the loss of a trait.

Taken together, these results indicate “that the once lost molecular blueprint of the male reproductive process may persist due to pleiotropic effects on other traits,” says Forni. “Different genes may undertake different preservation and degradation trajectories depending on the level of pleiotropy within the genetic regulatory network.”

This study not only sheds light on the persistence of genetic architecture after trait loss, but also offers potential insight into the emergence of rare males and cryptic sex (i.e., the episodic generation of males and sexual reproduction), which have been observed in an increasing number of lineages. they were thought to have long lost the ability to produce males. This opens up potential new avenues of research, with implications that could extend far beyond stick insects.

“It remains fundamental to examine the extent of genetic preservation following trait loss on a larger scale. Although the Bacillus species complex provides an interesting framework for resolving these issues, it would be useful to analyze a complex “broader species where multiple transitions between reproductive strategies have occurred,” notes Forni.

“While it is often necessary to rely on model species to discover and dissect 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 observing and analyzing the astonishing diversity of species. organisms and their complex adaptations.