Near-Stasis in the Long-Term Diversification of Mesozoic Tetrapods

Abstract

How did evolution generate the extraordinary diversity of vertebrates on land? Zero species are known prior to ~380 million years ago, and more than 30,000 are present today. An expansionist model suggests this was achieved by large and unbounded increases, leading to substantially greater diversity in the present than at any time in the geological past. This model contrasts starkly with empirical support for constrained diversification in marine animals, suggesting different macroevolutionary processes on land and in the sea. We quantify patterns of vertebrate standing diversity on land during the Mesozoic-early Paleogene interval, applying sample-standardization to a global fossil dataset containing 27,260 occurrences of 4,898 non-marine tetrapod species. Our results show a highly stable pattern of Mesozoic tetrapod diversity at regional and local levels, underpinned by a weakly positive, but near-zero, long-term net diversification rate over 190 million years. Species diversity of non-flying terrestrial tetrapods less than doubled over this interval, despite the origins of exceptionally diverse extant groups within mammals, squamates, amphibians, and dinosaurs. Therefore, although speciose groups of modern tetrapods have Mesozoic origins, rates of Mesozoic diversification inferred from the fossil record are slow compared to those inferred from molecular phylogenies. If high speciation rates did occur in the Mesozoic, then they seem to have been balanced by extinctions among older clades. An apparent 4-fold expansion of species richness after the Cretaceous/Paleogene (K/Pg) boundary deserves further examination in light of potential taxonomic biases, but is consistent with the hypothesis that global environmental disturbances such as mass extinction events can rapidly adjust limits to diversity by restructuring ecosystems, and suggests that the gradualistic evolutionary diversification of tetrapods was punctuated by brief but dramatic episodes of radiation.

Fig 1. Global counts of non-marine tetrapod taxa through time.

(A) Families (from [38]), (B) genera, and (C) species. Dashed lines are general linear models predicting taxon counts from geological age in mega-annum (Ma) for the entire Mesozoic, modelling taxon counts as a Poisson distribution and using a ln() link function (coefficients in Table 1). The data displayed in this figure can be accessed at http://doi.org/10.5061/dryad.9fr76 [48].

Fig 2. Regional counts of non-marine tetrapod taxa and fossil collections through time.

(A) Genera, (B) species, (C) collections yielding non-marine tetrapod fossils. Dashed lines in A and B are general linear models predicting taxon counts from geological age for the entire Mesozoic, modelling taxon counts as a Poisson distribution and using a ln() link function (coefficients in Table 2). The data displayed in this figure can be accessed at http://doi.org/10.5061/dryad.9fr76 [48].

Fig 3. “Global” non-marine tetrapod species diversity versus paleogeographic spread of fossil localities.

Using (A) genus counts, (B) subsampled genera, (C) species counts, and (D) subsampled species. Paleogeographic spreads are the minimum spanning tree lengths in km. Subsampled values were obtained using a quorum of 0.4. Correlation coefficients and p-values from Pearson’s correlation tests are reported in the top-left of each panel. Abbreviated interval names are given in full in S1 Table. The data displayed in this figure can be accessed at http://doi.org/10.5061/dryad.9fr76 [48].

Fig 4. Regional subsampled non-marine tetrapod species diversity versus paleogeographic spreads and paeolatitudinal centroids of fossil localities.

(A) Regional subsampled species diversity versus paleogeographic spread. (B) Regional subsampled species diversity versus paleolatitudinal centroid (positivised value). (C) Regional paleogeographic spreads versus geological age (Ma). (D) Regional paleolatitudinal centroids versus geological age (Ma). Paleogeographic spreads are the minimum spanning tree lengths in km. Subsampled values were obtained using a quorum of 0.4. Correlation coefficients and p-values from Pearson’s correlation tests are reported in the top-left panels A and B. Abbreviated interval names are given in full in S1 Table. The data displayed in this figure can be accessed at http://doi.org/10.5061/dryad.9fr76 [48].

Fig 5. Subsampled non-marine tetrapod species diversity.

(A) Subsampled species diversity within continental regions for a quorum of 0.4. The dashed line in A is the general linear model predicting subsampled regional diversity from geological age for the entire Mesozoic, modelling taxon counts as a Gaussian distribution and using a ln() link function (coefficients in Table 4). (B–D) Subsampled diversities for mammals (B), herps (C; non-mammalian, non-dinosaurian tetrapods), and dinosaurs (D). (E–G) Subsampling curves for (E) the Triassic–Early Jurassic of North America, Asia, and South Africa, (F) the Jurassic–Cretaceous of North America and Europe, and (G) the Cretaceous–Palaeogene of North America. The vertical, dashed grey lines in E–G indicate the target quorum of 0.4. An asterisk is placed in the same location of plots E–G to aid comparison. The data displayed in this figure can be accessed at http://doi.org/10.5061/dryad.9fr76 [48].

Fig 6. Within-locality alpha diversities of non-marine tetrapods and sampling methods against geological age.

(A) Alpha diversity excluding records that are indeterminate at the species level. (B) Alpha diversity including records that are indeterminate at the species level. (C) Per-interval global locality counts (black). (D) Per-interval global bulk sampled locality counts. In all panels, localities that have not been bulk sampled for microvertebrate remains are shown in grey and localities that have been bulk sampled are shown in red. The data displayed in this figure can be accessed at http://doi.org/10.5061/dryad.9fr76 [48].