Virgin-births may compromise species lifespan in the long term: a tale from lizards and snakes
Parthenogenesis is often seen as ecologically advantageous in the short term, but the rarity of this phenomenon in vertebrates points to long term disadvantages. Poster image: The family Lacertidae, here represented by Lacerta schreiberi, includes ~18% of parthenogenetic squamates. Credit: Hugo Maia
Our planet is a world of reptiles; at least when we think on vertebrates and when we think on terrestrial habitats. With more than 11,000 extant species, lizards and snakes (grouped in the Order Squamata) compete with birds in terms of species richness and ubiquity. However, unlike birds, some species of lizards and snakes have evolved virgin-births. In fact, these species are the only vertebrates with sperm-independent asexual reproduction, a phenomenon also known as parthenogenesis.
As part of my PhD research on diversification of lizards and snakes at the Centre for Marine and Environmental Studies (CESAM), University of Aveiro (Portugal), I came across this amazing fact: among all vertebrates with asexual reproduction, some lizards and snakes are the only ones that reproduce without the need for male fertilization. The ecological advantages of parthenogenesis are clear: it can lead to fast population increases; there is no need for mating; and parthenogens colonize environments that are unsuitable for sexual species. But then, why are there so few parthenogenetic species of Squamata? And why are those species relatively recent in the history of life? Parthenogenesis has only been described for 39 species of lizards and snakes so far, which represents only a small fraction of the entire clade. [FIGURE 1] Moreover, the low genetic diversity associated with parthenogenetic species could limit species adaptability to environmental changes. This suggests that parthenogenesis could be disadvantageous in the long-term, as no ancient species-rich clade of asexual species occurs in nature. Then, the concept of self-destructive traits came into help. A self-destructive trait is one that arises often but increases extinction rates or that is highly labile—frequently gained and lost. What if parthenogenesis is self-destructive for lizards and snakes? Shockingly, this hypothesis had not been examined.
Intrigued by these questions, and in collaboration with my PhD advisors Danny Rojas from the Pontificia Universidad Javeriana Cali (Colombia) and Carlos Fonseca also from CESAM, I did a thorough search to identify all described parthenogenetic species of Squamata. Afterwards, we chose two phylogenetic hypotheses and explored different metrics (namely, tip age rank sum, numbers of tips per origin, sum of sister clade differences and the Fritz and Purvis D statistic) and 9 macroevolutionary models that could provide evidence on the role of parthenogenesis as self-destructive. We would expect the following patterns: first, parthenogenetic species should be younger than sexual species; second, each origin of parthenogenesis should give rise to fewer than expected parthenogenetic species; third, parthenogenetic species should be scattered throughout the phylogeny; fourth, increased extinction rates should best explain the rarity found in nature given the long-term limitations of parthenogenesis. Overall, analyses could take as long as 2 days on a cluster server.
We found that parthenogenetic species are in fact younger than sexual species. Nevertheless, the number of species that originate from parthenogenetic ancestors is not lower than expected nor are the species more scattered across the phylogeny than expected. In summary, only scenarios that describe trait self-destruction could explain the macroevolutionary distribution of parthenogenetic species. These results highlight the role of parthenogenesis’ long-term disadvantages in shaping their rarity in nature. Higher extinction rates (but not trait lability) best explain the punctual occurrence of parthenogenesis in Squamata.
Our study recently out in Biology Letters opens new avenues. A follow-up study could examine, for example, the role of all forms of asexual reproduction in vertebrates, such as gynogenesis, hybridogenesis or kleptogenesis, as self-destructive traits. This could provide new insights on the evolution of asexual reproduction in vertebrates.