A second view on the evolution of flight in stick and leaf insects (Phasmatodea)

The re-evolution of complex characters is generally considered impossible, yet, studies of recent years have provided several examples of phenotypic reversals shown to violate Dollo's law. Along these lines, the regain of wings in stick and leaf insects (Phasmatodea) was hypothesised to have occurred several times independently after an ancestral loss, a scenario controversially discussed among evolutionary biologists. Here, we revisit the recovery of wings by reconstructing a phylogeny based on a comprehensive taxon sample of over 500 representative phasmatodean species to infer the evolutionary history of wings. We additionally explored the presence of ocelli, the photoreceptive organs used for flight stabilisation in winged insects, which might provide further information for interpreting flight evolution. Our findings support an ancestral loss of wings and that the ancestors of most major lineages were wingless. While the evolution of ocelli was estimated to be dependent on the presence of (fully-developed) wings, ocelli are nevertheless absent in the majority of all examined winged species and only appear in the members of few subordinate clades, albeit winged and volant taxa are found in every lineage. The disjunct distribution of ocelli substantiates the hypothesis on trait reacquisition and that wings were regained in Phasmatodea.

Return of a lost structure in the evolution of felid dentition revisited: A DevoEvo perspective on the irreversibility of evolution

There is a longstanding interest in whether the loss of complex characters is reversible (so-called “Dollo’s law”). Reevolution has been suggested for numerous traits but among the first was Kurtén (1963), who proposed that the presence of the second lower molar (M2) of the Eurasian lynx (Lynx lynx) was a violation of Dollo’s law because all other Felids lack M2. While an early and often cited example for the reevolution of a complex trait, Kurtén (1963) and Werdelin (1987) used an ad hoc parsimony argument to support their proposition that M2 reevolved in Eurasian lynx. Here I revisit the evidence that M2 reevolved in Eurasian lynx using explicit parsimony and maximum likelihood models of character evolution and find strong evidence that Kurtén (1963) and Werdelin (1987) were correct – M2 reevolved in Eurasian lynx. Next, I explore the developmental mechanisms which may explain this violation of Dollo’s law and suggest that the reevolution of lost complex traits may arise from the reevolution of cis-regulatory elements and protein-protein interactions, which have a longer half-life after silencing that protein coding genes. Finally, I present a model developmental model to explain the reevolution M2 in Eurasian lynx.

Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss

Dollo’s law posits that evolutionary losses are irreversible, thereby narrowing the potential paths of evolutionary change. While phenotypic reversals to ancestral states have been observed, little is known about their underlying genetic causes. The genomes of budding yeasts have been shaped by extensive reductive evolution, such as reduced genome sizes and the losses of metabolic capabilities. However, the extent and mechanisms of trait reacquisition after gene loss in yeasts have not been thoroughly studied. Here, through phylogenomic analyses, we reconstructed the evolutionary history of the yeast galactose utilization pathway and observed widespread and repeated losses of the ability to utilize galactose, which occurred concurrently with the losses of GALactose (GAL) utilization genes. Unexpectedly, we detected multiple galactose-utilizing lineages that were deeply embedded within clades that underwent ancient losses of galactose utilization. We show that at least two, and possibly three, lineages reacquired the GAL pathway via yeast-to-yeast horizontal gene transfer. Our results show how trait reacquisition can occur tens of millions of years after an initial loss via horizontal gene transfer from distant relatives. These findings demonstrate that the losses of complex traits and even whole pathways are not always evolutionary dead-ends, highlighting how reversals to ancestral states can occur.

Macroevolutionary Analyses Provide New Evidences of Phasmids Wings Evolution as a Reversible Process

The concept that complex ancestral traits can never be re-acquired after their loss has grown popular since its initial formulation and it’s often referred to as Dollo’s law. Nonetheless, several macroevolutionary evidences - along with molecular ones - suggest instances where complex phenotypes could have been lost throughout a clade evolutionary history and subsequently reverted to their former state in derived lineages. One of the first and most notable rejection of Dollo’s law is represented by wing evolution in phasmids: this polyneopteran order of insects - which comprises stick and leaf insects - has played a central role in initiating a long-standing debate on the topic. In this study, a new and comprehensive molecular phylogeny of over 300 Phasmatodea species is used as a framework for investigating wing’s evolutionary patterns in the clade, taking into consideration several sources of uncertainty and all the methodological recommendations which have been proposed to test Dollo’s law rejection. Macroevolutionary analyses support a dynamic and reversible evolution of wings, with multiple transitions to ancestral states taking place after their loss. Our findings suggest that neither wings or flight have acted as drivers of Phasmatodea species diversification and that brachyptery is an unstable state, when not co-opted for non-aerodynamic adaptations. We also explored the impact on our results of different assumptions relative to the probability of reversals and losses: we found that until reversals are assumed over 30 times more unlikely than losses, they are consistently inferred despite uncertainty in tree and model parameters. Our findings demonstrate that wings evolution can be a reversible and dynamic process in phasmids and contribute to shape our understanding of complex phenotypes evolution.

Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss

Dollo’s law posits that evolutionary losses are irreversible, thereby narrowing the potential paths of evolutionary change. While phenotypic reversals to ancestral states have been observed, little is known about their underlying genetic causes. The genomes of budding yeasts have been shaped by extensive reductive evolution, such as reduced genome sizes and the losses of metabolic capabilities. However, the extent and mechanisms of trait reacquisition after gene loss in yeasts have not been thoroughly studied. Here, through phylogenomic analyses, we reconstructed the evolutionary history of the yeast galactose utilization pathway and observed widespread and repeated losses of the ability to utilize galactose, which occurred concurrently with the losses of GALactose (GAL) utilization genes. Unexpectedly, we detected three galactose-utilizing lineages that were deeply embedded within clades that underwent ancient losses of galactose utilization. We show that at least two, and possibly three, lineages reacquired the GAL pathway via yeast-to-yeast horizontal gene transfer. Our results show how trait reacquisition can occur tens of millions of years after an initial loss via horizontal gene transfer from distant relatives. These findings demonstrate that the losses of complex traits and even whole pathways are not always evolutionary dead-ends, highlighting how reversals to ancestral states can occur.

Phenotypic plasticity explains violation of Dollo’s law

Dollo’s law of irreversibility states that once a complex adaptation has been lost in evolution, it will not be regained. Recently, various violations of this principle have been described. Here, we argue that the logic underlying Dollo’s law only applies to traits that are constitutively expressed, while it fails in case of ‘plastic’ traits that are up- or downregulated according to needs. We tested this hypothesis for an archetypal violation of Dollo’s law, the loss and regain of fat synthesis in parasitic wasps. Wasps from lineages that supposedly had lost lipogenic ability more than 200 million years ago were grown under various conditions. In line with our hypothesis, it turned out that fat synthesis had not been lost but was only switched on in low-fat environments. Such plasticity cannot only explain supposed violations of Dollo’s law, but also the maintenance of adaptations to rarely occurring extreme events.

Common lizards break Dollo’s law of irreversibility: genome-wide phylogenomics support a single origin of viviparity and re-evolution of oviparity

Dollo’s law of irreversibility states that once a complex trait has been lost in evolution, it cannot be regained. It is thought that complex epistatic interactions and developmental constraints impede the re-emergence of such a trait. Oviparous reproduction (egg-laying) requires the formation of an eggshell and represents an example of such a complex trait. In reptiles, viviparity (live-bearing) has evolved repeatedly but it is highly disputed if oviparity has re-evolved. Here, using up to 194,358 SNP loci and 1,334,760 bp of sequence, we reconstruct the phylogeny of viviparous and oviparous lineages of common lizards and infer the evolutionary history of parity modes. Our phylogeny strongly supports six main common lizard lineages that have been previously identified. We find very high statistical support for a topological arrangement that suggests a reversal to oviparity from viviparity. Our topology is consistent with highly differentiated chromosomal configurations between lineages, but disagrees with previous phylogenetic studies in some nodes. While we find high support for a reversal to oviparity, more genomic and developmental data are needed to robustly test this and assess the mechanism by which a reversal might have occurred.