Recent research on stick insects shows that genes associated with lost traits may be conserved across evolutionary timescales due to their multiple roles in biological processes, allowing for the potential reemergence of these traits. This study sheds light on the complex genetics of trait maintenance and reemergence, and points to broader implications for evolutionary biology.
Recent research shows that genes associated with lost traits may be retained in stick insects, allowing for their potential return over evolutionary time.
Traits can disappear through evolution if they become unnecessary or require too many resources to maintain. It is widely thought that the genes associated with these traits will also deteriorate over time, possibly preventing the traits from reappearing. However, there are countless examples in nature of once-lost traits reappearing in descendants.
According to Giobbe Forni, a Research Fellow at the University of Bologna: “Mapping the presence and absence of traits on a kind tree suggests that some traits were lost in the lineages that led to extant species and then recovered. Wings on stick insects are considered one of the most iconic examples of this evolutionary process.”
This suggests that the genes associated with these traits may be preserved for millions of years. However, there has been limited research into the molecular basis of this reemergence, meaning that the mechanisms responsible for the maintenance of these genes remain largely speculative to date.
New insights from genetic studies
From a new study published in Genome biology and evolution, Forni and his colleagues shed light on another complex trait that has been lost in some stick insects: the production of males. Loss of the ability to produce males results in populations of only 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 persist long after a trait is lost, providing a potential opportunity for trait reemergence over long evolutionary timescales.
A stick bug.
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 Bacillus grandii marettimi populations consist of males and females that reproduce sexually, Bacillus atticus populations have lost the ability to produce males, and consist only of females that reproduce through parthenogenesis. A third kind, Bacillus Rossius, includes both sexual populations and parthenogenetic populations that have lost the ability to produce males. By studying the fate of genes involved in male reproduction in these three species, the authors sought to investigate the extent to which genes are retained after trait loss and the possible mechanisms driving this retention.
Surprising findings in gene conservation
The researchers first identified gene networks whose expression was correlated with male or female reproduction in the sexual species B. marettimi and then evaluated the same genes B. atticus And B. Rossius. Surprisingly, male-related genes showed no signs of weakened selection or accelerated evolution compared to female-related genes in the parthenogenetic species. Furthermore, male-related patterns of gene expression were partially conserved across both parthenogenetic species.
Digging deeper, the researchers found that genes in female-related networks were expressed primarily in female reproductive tissues, while those in male-related networks were expressed in male genes. And female reproductive tissues, including both sexual and parthenogenetic females. This suggests that male 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 could explain the conservation of male genes in these parthenogenetic stick insects, as previously hypothesized.
Photo of a stick insect. Credit: Filippo Castellucci
Furthermore, the authors found that genes that were strongly 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 gene retention after trait loss. Taken together, these findings indicate that “the molecular basis of the once-lost male reproductive process may persist due to pleiotropic effects on other traits,” Forni explains. “Different genes may follow different trajectories of maintenance 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 potential insight into the emergence of rare males and cryptic sex (i.e. episodic generation of males and sexual reproduction), which have been observed in a increasing number of genera that were thought to have long since lost the ability to produce males. This opens up new potential avenues for research, with implications that could extend far beyond stick insects.
“Looking at how widespread genetic conservation occurs after trait loss on a larger scale remains fundamental. Although the Bacillus species complex offers a nice framework to tackle these problems. It would be useful to analyze a larger species complex 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 make more efforts to observe and analyze the astonishing diversity of organisms and their complex adaptations.”
Reference: “Parthenogenetic stick insects show signatures of conservation in the molecular architecture of male reproduction” by Giobbe Forni, Barbara Mantovani, Alexander S Mikheyev and Andrea Luchetti, April 4, 2024, Genome biology and evolution.
DOI: 10.1093/gbe/evae073