Epoch‐based likelihood models reveal no evidence for accelerated evolution of viviparity in squamate reptiles in response to cenozoic climate change

Abstract

A broad scale analysis of the evolution of viviparity across nearly 4,000 species of squamates revealed that origins increase in frequency toward the present, raising the question of whether rates of change have accelerated. We here use simulations to show that the increased frequency is within the range expected given that the number of squamate lineages also increases with time. Novel, epoch-based methods implemented in BEAST (which allow rates of discrete character evolution to vary across time-slices) also give congruent results, with recent epochs having very similar rates to older epochs. Thus, contrary to expectations, there was no accelerated burst of origins of viviparity in response to global cooling during the Cenozoic or glacial cycles during the Plio-Pleistocene. However, if one accepts the conventional view that viviparity is more likely to evolve than to be lost, and also the evidence here that viviparity has evolved with similar regularity throughout the last 200 Ma, then the absence of large, ancient clades of viviparous squamates (analogs to therian mammals) requires explanation. Viviparous squamate lineages might be more prone to extinction than are oviparous lineages, due to their prevalance at high elevations and latitudes and thus greater susceptibility to climate fluctuations. If so, the directional bias in character evolution would be offset by the bias in extinction rates.

Evolutionary origins of viviparity consistent with palaeoclimate and lineage diversification

“…Transitions to viviparity coincided with diversification of squamate reptiles in general, casting doubt on whether climate alone is enough to either explain or manifest the evolution of viviparity. Our result is consistent with a previous study concluding that transitions to viviparity had not occurred more frequently than expected during cold epochs within the last 65 million years (King & Lee, 2015). One reason for the association between origins of viviparity and diversification could be that transitions to viviparity favour diversification.…”

“…One reason for the association between origins of viviparity and diversification could be that transitions to viviparity favour diversification. This has been previously suggested for squamate reptiles (Lambert & Wiens, 2013), although extinction rates were also higher for viviparous species (King & Lee, 2015; Pyron & Burbrink, 2014). In addition, origins of viviparity did not lead to phenotypic diversification in phrynosomatid lizards (Zúñiga‐Vega et al., 2016).…”

“…Reversals to oviparity from viviparity involve re‐evolving egg‐shells and were thought to be unlikely or impossible (Pincheira‐Donoso et al., 2013; Shine, 2005; Sites et al., 2011); there are few reported convincing cases (Lynch & Wagner, 2010; Recknagel et al., 2018). However, the potential for reversals is still disputed and recent studies have proposed that reversals to oviparity have occurred more frequently but still rarely (Blackburn, 2015; Fenwick et al., 2012; King & Lee, 2015; Pyron & Burbrink, 2014). Therefore, we did not include potential transitions from viviparity to oviparity in our analysis.…”

Advancing perspectives on parity‐mode evolution

“…When we submitted our manuscript (Pyron and Burbrink, ) on 2 May 2013, I did not anticipate how controversially it would be received, or the magnitude of the response. Articles in this issue (Blackburn, ,b; Duchêne and Lanfear, ; Griffith et al, ; King and Lee, ; Shine, ; Stewart, ; Wright et al, ) and in other journals (King and Lee, ) have re‐examined our data, analyses, and conclusions, drawing a wide range of inferences. Our summary (Pyron and Burbrink, ) was written before any of the responses appeared, and merely gives an overview of our original conclusions, with some suggestions for future research.…”

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

“…However, there is little evidence for the existence of reversals to oviparity (Griffith et al, 2015). Original claims for reversals from viviparity to oviparity have been made based on the presence of oviparous lineages embedded in viviparous lineages (e.g., de Fraipont, Clobert, & Barbault, 1996;Pyron & Burbrink, 2014), but subsequent work refuted these claims based on analytical problems, data problems (e.g., Blackburn, 1999;Lee & Shine, 1998;Shine & Lee, 1999), and other grounds (Blackburn, 2015;Duchêne & Lanferar, 2015;Griffith et al, 2015;King & Lee, 2015;Mank, Promislow, & Avise, 2005;Parenti, LoNostro, & Grier, 2010;Pyron, 2015;Shine, 2015;Wright, Lyons, Brandley, & Hillis, 2015).…”