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

Abstract

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 can re-evolve. 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 supports six main common lizard lineages that have been previously identified. We find strong 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.

Reversals in complex traits uncovered as reticulation events: Lessons from the evolution of parity‐mode, chromosome morphology, and maternal resource transfer

“…In Z. vivipara, the level-1 network unraveled clade F as a reticulation ( Figure 2C) between a lineage with fused autosome and a lineage, which conserved the ancestral W-chromosome morphology ( Figure 3C). The reticulate origin of clade F coincides with a recently published study pointing to important past migration events in clade F (Recknagel, Kamenos, & Elmer, 2018;Fig S4D-F see CV2: central viviparous clade, which corresponds to clade F, Surget-Groba et al, 2006).…”

“…A. eryth depicts the outgroup and refers to the closest species with known W chromosome morphology: Acanthodactylus erythrurus 2016). While for the Cyprinodontiformes no genomic analyses were available, for Z. vivipara genomic analyses based on 1.3 million base pairs (~200′000 SNP loci) were congruent with a reversal from viviparity to oviparity in clade B (Recknagel et al, 2018) and they did not unravel important past migration ( Figure S4 in Recknagel et al, 2018; WOV corresponds to clade B). Consequently, only one of them here studied potential reversals may have originated by means of small evolutionary steps (reversal to oviparity in clade B), three reversals may exist due to reticulation, and one reversal is of unknown origin and requires future investigation (P. elongate).…”

Distinct telomere differences within a reproductively bimodal common lizard population

“…To do so, we followed the ddRADSeq library preparation protocol of Recknagel et al (2018); see Appendix S1 for details.…”

“…Reproductive mode in this species is known to be genetically determined and fixed between lineages (Arrayago, Bea, & Heulin, 1996;Recknagel, Kamenos, & Elmer, 2018). The oviparous mothers lay calcified eggs ~33 days after copulation (i.e.…”

Facultative oviparity in a viviparous skink ( Saiphos equalis )

“…Reversals from viviparity to oviparity are rare [3][4][5][6], yet recent phylogenetic work suggesting frequent reversals [7] has rekindled debate about their adaptive significance for squamate evolution. Dollo's Law of irreversibility predicts that complex traits, once lost, either cannot re-evolve or will do so in a different way [3,5,8,9]. The evolution of viviparity involves loss of complex structures, including the eggshell and oviductal glands that produce shell material, and requires changes in maternal vasculature and timing of reproductive events [8].…”