The origins of modern biodiversity on land

Abstract

Comparative studies of large phylogenies of living and extinct groups have shown that most biodiversity arises from a small number of highly species-rich clades. To understand biodiversity, it is important to examine the history of these clades on geological time scales. This is part of a distinct 'phylogenetic expansion' view of macroevolution, and contrasts with the alternative, non-phylogenetic 'equilibrium' approach to the history of biodiversity. The latter viewpoint focuses on density-dependent models in which all life is described by a single global-scale model, and a case is made here that this approach may be less successful at representing the shape of the evolution of life than the phylogenetic expansion approach. The terrestrial fossil record is patchy, but is adequate for coarse-scale studies of groups such as vertebrates that possess fossilizable hard parts. New methods in phylogenetic analysis, morphometrics and the study of exceptional biotas allow new approaches. Models for diversity regulation through time range from the entirely biotic to the entirely physical, with many intermediates. Tetrapod diversity has risen as a result of the expansion of ecospace, rather than niche subdivision or regional-scale endemicity resulting from continental break-up. Tetrapod communities on land have been remarkably stable and have changed only when there was a revolution in floras (such as the demise of the Carboniferous coal forests, or the Cretaceous radiation of angiosperms) or following particularly severe mass extinction events, such as that at the end of the Permian.

Figure 1.

Changes through time in some key environmental parameters and in terrestrial tetrapod diversification. The curves, all plotted against the Phanerozoic time scale (left-hand side), show the percentage oxygen, carbon dioxide (in parts per million, ppm), the average global temperature (in degrees Celsius, °C), sea-level change (in metres difference above, or below, present levels) and the number of continents. Tetrapod diversification is documented as change in number of families and in number of major ecological modes (‘guilds’) documented in ecosystems. Sources of information: O₂ data from Berner (2003), CO₂ and temperature data from Royer et al. (2004), sea-level data from Haq & Schutter (2008), number of continents counted from the Scotese Paleomap website, http://www.scotese.com/, and tetrapod diversity and number of occupied niches from Sahney et al. (2010).

Figure 2.

Ecological role of tetrapods through time. (a) The average number of tetrapod families occupying a single mode and the global taxonomic diversity of the different tetrapod classes. Black curve, families per mode; dashed dark blue curve, mammals; dashed light blue curve, birds; dotted green curve, reptiles; dotted grey curve, amphibians. (b) Rate of expansion/contraction of mode utilization and the general ‘normal’ range of this rate (shaded area) with the exception of troughs and peaks at major extinction events. Mass extinctions are labelled as (1) end-Permian mass extinction, (2) end-Triassic mass extinction, (3) end-Cretaceous mass extinction, and (4) Grande Coupure. Neo, Neogene; Paleo, Paleogene. Based on Sahney et al. (2010).

Figure 3.

Comparison of (a) neocete, (b) mysticete and (c) odontocete (d) diversity with diatom diversity and (e) global δ¹⁸O values through the past 30 Myr. Cetacean diversity is shown as sampled-in-bin data as downloaded from the Paleobiology Database (grey) and as a ranged-through estimate (black). Error for the δ¹⁸O curve is shown as mean standard error (s.e.) multiplied by 100. Based on Marx & Uhen (2010), with permission from the American Association for the Advancement of Science.

Figure 4.

Cosmopolitanism of tetrapods through the Carboniferous, Permian and Triassic. Cosmopolitanism (C) is measured as mean alpha diversity () divided by global diversity (Tt), according to the formula C = /Tt. The bars are total ranges of values for each time bin. Note the overall decline of cosmopolitanism through this time interval, perhaps related to increasing taxonomic and ecological diversity of tetrapods, but also note the coupled rises and falls in cosmopolitanism following major extinction events, especially Olson's extinction (1), the end-Guadalupian extinction (2), and the end-Permian extinction (3). Cisur, Cisuralian; ET, Early Triassic; Guad, Guadalupian; Lopin, Lopingian; LT, Late Triassic; Miss, Mississippian; MTr, Middle Triassic; Penn, Pennsylvanian. Based on Sahney & Benton (2008).

Figure 5.

Phylogenetic study of dinosaurian origins, showing the interplay of diversity and disparity increase in an expanding clade, associated with changes in relative abundance. The phylogeny (a) shows much branching of major lineages in the Middle Triassic (Anisian, Ladinian) and Late Triassic (Carnian, Norian, Rhaetian). Vertical dashed lines mark the Carnian–Norian turnover, when many key tetrapods, especially herbivores, died out, and the end-Triassic mass extinction, and these extend through the comparison of key measures of evolutionary change among these archosaurs (b), namely diversity (counts of genera, phylogenetically corrected), disparity (sum of ranges) and morphological evolutionary rates (patristic dissimilarity per branch/time). Error bars on disparity values represent 95% bootstrap confidence intervals, and non-overlapping error bars indicate a significant difference between two time-bin comparisons. Question mark indicates uncertain rate measure for Early Jurassic archosaurs. Two patterns are shown: the major increase in archosaur disparity (Carnian) occurred before the main increase in diversity (Norian), and archosaur morphological rates were highest early in the Triassic, before the disparity and diversity spikes. (c) Relative abundance of four key groups in individual well-sampled faunas shows major changes in proportions through the Triassic, as synapsids are replaced by basal archosaurs and ultimately dinosaurs, as the dominant elements. (d) Morphospace plots for archosaurs in the (i) Late Triassic (Carnian–Norian) and (ii) Early Jurassic (Hettangian–Toarcian), showing the first two principal coordinates (shape axes). Crurotarsans had a larger morphospace than dinosaurs in the Late Triassic, but these roles were reversed in the Early Jurassic after crurotarsan morphospace occupation crashed. ET, Early Triassic; Rht, Rhaetian. Data modified from (a) Brusatte et al. (2010a), (b) Brusatte et al. (in press), (c) Benton (1983), and (d) Brusatte et al. (2010b).