Biogeography of worm lizards (Amphisbaenia) driven by end-Cretaceous mass extinction

Abstract

Worm lizards (Amphisbaenia) are burrowing squamates that live as subterranean predators. Their underground existence should limit dispersal, yet they are widespread throughout the Americas, Europe and Africa. This pattern was traditionally explained by continental drift, but molecular clocks suggest a Cenozoic diversification, long after the break-up of Pangaea, implying dispersal. Here, we describe primitive amphisbaenians from the North American Palaeocene, including the oldest known amphisbaenian, and provide new and older molecular divergence estimates for the clade, showing that worm lizards originated in North America, then radiated and dispersed in the Palaeogene following the Cretaceous-Palaeogene (K-Pg) extinction. This scenario implies at least three trans-oceanic dispersals: from North America to Europe, from North America to Africa and from Africa to South America. Amphisbaenians provide a striking case study in biogeography, suggesting that the role of continental drift in biogeography may be overstated. Instead, these patterns support Darwin and Wallace's hypothesis that the geographical ranges of modern clades result from dispersal, including oceanic rafting. Mass extinctions may facilitate dispersal events by eliminating competitors and predators that would otherwise hinder establishment of dispersing populations, removing biotic barriers to dispersal.

Keywords: adaptive radiation; dispersal; evolution; mass extinction.

Figure 1.

Fossils of Palaeocene Amphisbaenia from North America. (a–c) Chthonophis subterraneus, AMNH 30799, holotype right dentary: (a) medial view, (b) dorsal view and (c) lateral view. (d–f) Archaerhineura mephitis, YPM 18627, holotype right dentary: (d) lateral view, (e) medial view and (f) dorsal view. (g–i) Oligodontosaurus cf. wyomingensis, YPM-PU 16777 left dentary: (g) lateral view, (h) medial view and (i) dorsal view. Abbreviations: af, adductor fossa; cof, coronoid facet; cop, coronoid process; fa, facet for articular; mc, Meckelian canal; mf, mental foramina; nf, nutrient foramen; spf, splenial facet; sym, symphysis.

Figure 2.

Phylogenetic analysis of Amphisbaenia. (a) Results of Bayesian analysis of five genes (16S, BDNF, CMOS, ND2 and RAG1) using CAT-GTR in PhyloBayes 3.3f. (b) Results of morphological analysis, using molecular data as a constraint.

Figure 3.

Divergence dates for molecular clock analyses, showing post K–Pg radiation. (a) CIR hard bounds, fossil minima only, (b) CIR soft bounds, minima and maxima, (c) uncorrelated gamma multipliers, fossil minima only, and (d) CIR soft bounds, minima and maxima, only calibrations external to Amphisbaenia. Red line and blue band represent the K–Pg boundary and break-up of Pangaea, respectively. Red vertical bars indicate 95% CIs for diversification of the main radiation of Amphisbaenia, the Amphisbaeniformes. In all cases, the 95% CI overlaps the K–Pg boundary consistent with post-Cretaceous diversification of Amphisbaenia, but fails to overlap the formation of the Atlantic Ocean, rejecting (p < 0.05) the hypothesis that vicariance drove amphisbaenian diversification.

Figure 4.

Comparison of fossil- and vicariance-calibrated molecular divergence estimates. (a) Calibrated using fossil minima and maxima, (b) calibrated using the connection of the North and South Atlantic ca 100 Ma to date the divergence of African and South American Amphisbaenia.

Figure 5.

Phylogeny of Amphisbaenia. The basal position of the rhineurids and the Palaeocene Chthonophis and Oligodontosaurus are consistent with a North American origin of Amphisbaenia. The rapid appearance of new lineages in the Palaeocene documents post-Chicxulub radiation. The radiation is associated with multiple dispersal events—colonization of Europe by Blanidae, Africa by Afrobaenia and South America by Amphisbaenidae. Strict consensus of 76 trees, based on an analysis of 48 taxa and 310 characters using a molecular tree as a backbone constraint. See the electronic supplementary material for details.

Figure 6.

Oceanic dispersal of Amphisbaenia. Multiple oceanic dispersal events are implied by the phylogeny recovered here: (1) dispersal of Blanidae from North America to Europe; (2) dispersal of stem Afrobaenia from North America to Africa; (3) dispersal of Cadeidae to Cuba (either from Africa, as shown, or else from North America); (4) dispersal of Amphisbaeninae to South America; and (5) dispersal of Amphisbaeninae through the Caribbean.