Mesozoic mammaliaform diversity: The effect of sampling corrections on reconstructions of evolutionary dynamics
Introduction
For decades, the focus of synapsid palaeontology has been on the therapsid response and recovery to the end Permian mass extinction, and the mammalian radiation following the K/Pg mass extinction, which heralded the “Age of Mammals”. However, the fossil record of Mesozoic mammaliaforms spans ~ 2.5 times the duration of the comparatively well-studied record of Cenozoic mammals. Within Mammaliaformes, 11 major clades or functional grades (following Kielan-Jaworowska et al., 2004, and detailed below) formed an ecologically diverse Mesozoic assemblage from the Carnian (Late Triassic, ca 235–229 mya) onwards (Luo, 2007a). Recent fossil discoveries highlight a complex evolutionary history for Mesozoic Mammaliaformes (e.g. Luo et al., 2011), with the traditional scenario of a linear acquisition of mammalian characters being challenged by multiple evolutionary origins of key morphological features such as the tribosphenic molar (Luo et al., 2001) and middle ear ossicles (Luo et al., 2011). Moreover, in contrast to common depictions of early mammaliaforms as small terrestrial and scansorial insectivores, new fossils demonstrate that Mesozoic mammaliaforms invaded a variety of ecological niches, from semi-aquatic to gliding forms, and even dog-sized forms that preyed on juvenile dinosaurs (Hu et al., 2005, Luo and Wible, 2005, Ji et al., 2006, Meng et al., 2006, Luo, 2007a). Despite the great attention paid in recent years to this previously unappreciated morphological and ecological diversity of early mammaliaforms, and a series of recent quantitative studies of taxonomic diversity in more basal synapsids (Brocklehurst and Fröbisch, 2014, Brocklehurst et al., 2013, Fröbisch, 2013), there has been little rigorous analysis of mammaliaform diversity dynamics prior to the K/Pg mass extinction (Rose, 2006). Previous approaches have been either broad and qualitative assessments of subclades (Luo, 2007b) or geographically restricted to the North American record (Alroy, 2009) and more specific localities (Wilson, 2005, Wilson, 2013).
Reconstructing diversity dynamics over deep time is a core theme of palaeobiology (Jablonski, 1999, Raup, 1972, Valentine, 1985). Although the potential effects of geological and anthropogenic biases on accurate taxon counts have been discussed for decades (Raup et al., 1975), it is only more recently that substantial efforts have been made to correct these biases (Alroy, 2000, Alroy, 2008, Alroy, 2010, Alroy et al., 2001, Alroy et al., 2008, Behrensmeyer et al., 2005, Peters and Foote, 2001, Smith and McGowan, 2007, Smith et al., 2012). A growing number of studies have focussed in particular on biases introduced by differences in outcropping rock area (Crampton et al., 2003, Smith and McGowan, 2007), preservation potential of fossil organisms (Smith, 2001), or evenness and fairness of sampling during standard intervals (Alroy, 2010, Alroy et al., 2001, Alroy et al., 2008). These studies suggest that many features of observed diversity curves could be artefacts of changes in fossil preservation, geological sampling, or anthropogenic sampling rather than true biotic signals (e.g. Smith, 2007, Smith et al., 2012). Complex Earth system interactions such as sea level change may drive both sedimentation and ancient biodiversity in the marine realm, suggesting that covariation of fossil taxon counts and potentially biasing factors is not always causal (Peters, 2005, Benson and Butler, 2011, Hannisdal and Peters, 2011; but see Smith and Benson, 2013). However, terrestrial processes may be simpler, with factors such as rock area and collection effort directly biasing taxon counts (e.g. Benson and Upchurch, 2013, Benson et al., 2013, Butler et al., 2011a, Butler et al., 2011b, Upchurch et al., 2011). Here, we present the first quantitative investigation of the global taxonomic palaeodiversity of Mesozoic Mammaliaformes, applying robust sampling-correction approaches to account for geological and anthropogenic biases and reassessing diversity dynamics in early mammal evolution.
Section snippets
Mammaliaform taxa
We have attempted to maximise coverage of Mesozoic mammaliaform occurrence data in the Palaeobiology Database (Alroy et al., 1998), with an extensive literature review and comparison with data in Kielan-Jaworowska et al. (2004). Mammaliaformes was considered as a monophyletic clade, consisting of all descendants of the most recent common ancestor of Morganucodonta and crown Mammalia (Luo et al., 2002, Rowe, 1988, Zhou et al., 2013). Morganucodonts, docodonts and kuehneotherids are successively
Observed Mesozoic mammaliaform taxonomic diversity
We first calculated observed in-bin species counts (species taxonomic diversity estimate; STDE) and generic counts (generic taxonomic diversity estimate; GTDE) (Table 1). The uncorrected mammaliform fossil record displays an apparent long-term increase in diversity through the Mesozoic, punctuated by four peaks occurring in the Late Triassic (Triassic 4), Late Jurassic (Jurassic 6), early Late Cretaceous (Cretaceous 3) and Late Cretaceous (Cretaceous 6–7) (Fig. 1a). These peaks are separated by
Sampling bias in the mammaliaform fossil record
The significant correlations between observed mammaliaform diversity and multiple fossil sampling proxies suggest that some patterns in apparent diversity may be explained by temporal variation in rock record quality rather than by evolutionary dynamics. As a result, caution is needed when interpreting uncorrected data. Both sets of analyses described here do support discrete series of statistically robust shifts in Mesozoic mammaliaform diversity. However, it is important to note that these
Acknowledgements
We acknowledge the substantial work by contributors of the Paleobiology Database (http://paleodb.org), especially John Alroy and Matthew Carrano. We thank John Alroy for his considerable guidance when initially running the SQS analyses. This work was supported by a Leverhulme Research Project Grant (RPG-129) to PU and AG. Finally, we thank all those who reviewed our original manuscript. This paper is Palaeobiology database publication number #204.
References (85)
- et al.
Cretaceous tetrapod fossil record sampling and faunal turnover: implications for biogeography and the rise of modern clades
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2013) - et al.
The first half of tetrapod evolution, sampling proxies, and fossil record quality
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2013) - et al.
Current and historical perspectives on the completeness of the fossil record of pelycosaurian-grade synapsids
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2014) - et al.
Possible persistence of the morganucodontans in the Lower Cretaceous Purbeck Limestone Group Dorset, England
Cretac. Res.
(2012) Vertebrate diversity across the end-Permian mass extinction—separating biological and geological signals
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2013)- et al.
Model selection in ecology and evolution
Trends Ecol. Evol.
(2004) - et al.
The nonmarine Lower Cretaceous of the North American Western Interior foreland basin: new biostratigraphic results from ostracod correlations and early mammals, and their implications for paleontology and geology of the basin — an overview
Earth Sci. Rev.
(2010) New methods for quantifying macroevolutionary patterns and processes
Paleobiology
(2000)Dynamics of origination and extinction in the marine fossil record
Proc. Natl. Acad. Sci. U. S. A.
(2008)Speciation and extinction in the fossil record of North American mammals
Geographical, environmental and intrinsic biotic controls on Phanerozoic marine diversification
Palaeontology
The palaeobiology database
Effects of sampling standardization on estimates of Phanerozoic marine diversification
Proc. Natl. Acad. Sci. U. S. A.
Phanerozoic trends in the global diversity of marine invertebrates
Science
Sedimentology, stratigraphy, and extinctions during the Cretaceous–Paleogene transition at Bug-Creek, Montana — comment
Geology
Cretaceous extinctions: multiple causes
Science
Dinosaur diversity and the rock record
Proc. R. Soc. B Biol. Sci.
Are the most durable shelly taxa also the most common in the marine fossil record?
Paleobiology
Controlling the false discovery rate — a practical and powerful approach to multiple testing
J. R. Stat. Soc. Ser. B Methodol.
Uncovering the diversification history of marine tetrapods: ecology influences the effect of geological sampling biases
Geol. Soc. Lond., Spec. Publ.
Faunal turnover of marine tetrapods during the Jurassic–Cretaceous transition
Biol. Rev.
Diversity trends in the establishment of terrestrial vertebrate ecosystems: interactions between spatial and temporal sampling biases
Geology
Assessing the quality of the fossil record: insights from vertebrates
Geol. Soc. Lond., Spec. Publ.
The completeness of the fossil record of Mesozoic birds: implications for early avian evolution
Plos One
The early evolution of synapsids, and the influence on their fossil record
Paleobiology
Dinosaur morphological diversity and the end-Cretaceous extinction
Nat. Commun.
Diversity patterns amongst herbivorous dinosaurs and plants during the Cretaceous: implications for hypotheses of dinosaur/angiosperm co-evolution
J. Evol. Biol.
The taxonomic diversity and morphological disparity of pterosaurs: untangling sampling biases, the impact of Lagerstatten, and diversification trajectories
J. Vertebr. Paleontol.
Sea level, dinosaur diversity and sampling biases: investigating the ‘common cause’ hypothesis in the terrestrial realm
Proc. R. Soc. B Biol. Sci.
Estimating the rock volume bias in paleobiodiversity studies
Science
Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny
Proc. R. Soc. B Biol. Sci.
Molecular dating and biogeography of the early placental mammal radiation
J. Hered.
The extinction of the dinosaurs in North America
GSA Today
Shape of Mesozoic dinosaur richness
Geology
Evolutionary and preservational constraints on origins of biologic groups: divergence times of eutherian mammals
Science
a Middle Jurassic mammal bed from Oxfordshire
Palaeontology
Global taxonomic diversity of anomodonts (Tetrapoda, Therapsida) and the terrestrial rock record across the Permian–Triassic boundary
Plos One
The population frequencies of species and the estimation of population parameters
Biometrika
A dating success story: genomes and fossils converge on placental mammal origins
Evodevo
A radiation of arboreal basal eutherian mammals beginning in the Late Cretaceous of India
Proc. Natl. Acad. Sci. U. S. A.
Mammal disparity decreases during the Cretaceous angiosperm radiation
Proc. R. Soc. B
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