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Four Mammal Fossil Calibrations: Balancing Competing Palaeontological and Molecular Considerations

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Four Mammal Fossil Calibrations: Balancing Competing Palaeontological and Molecular Considerations Palaeontologia Electronica palaeo-electronica.org Four mammal fossil calibrations: balancing competing palaeontological and molecular considerations Matthew J. Phillips ABSTRACT With the introduction of relaxed-clock molecular dating methods, the role of fossil calibration has expanded from providing a timescale, to also informing the models for molecular rate variation across the phylogeny. Here I suggest fossil calibration bounds for four mammal clades, Monotremata (platypus and echidnas), Macropodoidea (kan- garoos and potoroos), Caviomorpha-Phiomorpha (South American and African hystricognath rodents), and Chiroptera (bats). In each case I consider sources of uncertainty in the fossil record and provide a molecular dating analysis to examine how the suggested calibration priors are further informed by other mammal fossil calibra- tions and molecular data. Matthew J. Phillips. School of Earth, Environmental and Biological Sciences, Queensland University of Technology, 2 George Street, Brisbane 4000, Australia, [email protected] Keywords: Caviomorpha-Phiomorpha; Chiroptera; fossil calibration; Macropodoidea; Monotremata; molecular dating INTRODUCTION cal workers are increasingly working together to frame calibration procedures (Ksepka et al., 2011; The use of fossils to calibrate molecular evo- Parham et al., 2012) to consider the sources of lutionary timescales has become increasingly com- error attributable to fossil records within the context plex over the past decade. Single point calibrations of modern molecular dating methods. have been superseded by multiple sets of calibra- Many mammalian molecular dating studies tion bounds, which in turn are often modelled in continue to rely heavily on identifying the oldest Bayesian analyses as prior (e.g., uniform, normal, members of clades by searching reference classifi- lognormal) distributions between minimum and cations (e.g., McKenna and Bell, 1997) that were maximum ages (see Ho and Phillips, 2009). In step not intended as calibration sources and include with these changes, molecular and palaeontologi- PE Article Number: 18.1.5FC Copyright: Palaeontological Association February 2015 Submission: 13 May 2014. Acceptance: 19 June 2014 Phillips, Matthew J. 2014. Four mammal fossil calibrations: balancing competing palaeontological and molecular considerations. Palaeontologia Electronica 18.1.5FC; 1-16; palaeo-electronica.org/content/content/fc-5 Calibrations published in the Fossil Calibration Series are accessioned into the Fossil Calibration Database (www.fossilcalibrations.org). The Database is a dynamic tool for finding up-to-date calibrations, and calibration data will be updated and annotated as interpretations change. In contrast, the Fossil Calibration papers are a permanent published record of the information on which the calibrations were originally based. Please refer to the Database for the latest data. PHILLIPS: FOUR MAMMAL CALIBRATIONS many poorly known taxa. Calibration compilations dating estimates among placental mammals more such as Benton et al. (2009) have begun to over- broadly (Springer et al., 2003; Waddell, 2008; haul this practice and reflect diverse considerations Welch et al., 2008; Steiper and Seiffert, 2012). The that need to be applied to justifying calibration recently published oldest record for South Ameri- bounds. Here I suggest calibration bounds for four can rodents (Antoine et al., 2011) permits the new widely separated mammalian crown clades that Caviomorpha-Phiomorpha calibration, while phylo- were not considered by Benton et al. (2009): genetic and fossil record improvements over the Monotremata (platypus and echidnas), Macropo- past decade (see Teeling et al., 2005; Eiting and doidea (kangaroos and potoroos), Caviomorpha- Gunnell, 2009) allow re-evaluation of crown Chi- Phiomorpha (African and South American roptera calibration. hystricognath rodents), and Chiroptera (bats). The development of calibration strategies has The Australian terrestrial mammal fossil carefully considered uncertainties associated with record includes a 30 Ma hiatus from the earliest the fossil record and its interpretation for placing Eocene through to the latest Oligocene (Black et both minimum and maximum bounds on nodes al., 2012). The earlier fossils, although including (e.g., Reisz and Müller, 2004; Benton and Dono- crown marsupials, do not clearly fit into modern ghue, 2007). More attention, however, may need to orders (Beck et al., 2008), while many calibrations be paid to how fossil calibrations interact with each derived from the latest Oligocene faunas (e.g., other and with the evolutionary models that under- Vombatiformes and Phalangeroidea) are expected pin molecular dating (Ho and Phillips; 2009; Pyron, to substantially postdate the actual divergence 2010; Warnock et al., 2012). These interactions times (Meredith et al., 2009, Black et al., 2012). In have become more important due to recent devel- contrast, records from the latest Oligocene to Early opments in molecular dating and have implications Miocene include numerous ‘transitional’ macropo- for balancing the imperative to closely calibrate doids morphologically close to expectations for the divergences with the need to avoid erroneous cali- kangaroo-potoroo divergence (Prideaux and War- brations. burton, 2010). Hence, Macropodoidea likely pro- One important molecular dating development vides one of the most informative calibrations is that universal clocks have given way to ‘relaxed above the family level among Australian marsupi- clock’ methods that model variation in molecular als. evolutionary rates across the phylogeny (see Sparse Australian mammal fossil records Welch and Bromham, 2005). Sets of calibration have also hampered calibration of Monotremata, bounds now simultaneously calibrate molecular with minimum age suggestions ranging from 15.92 divergence and substantially inform the model for Ma (Beck et al., 2008) to 121 Ma (Rowe et al., how rates of molecular evolution vary across the 2008). The platypus (Ornithorhynchidae) morpho- phylogeny. This rate variation is typically assumed type extends at least back to the Paleocene to follow a specific distribution (e.g., lognormal) (Monotrematum, Pascual et al., 1992), while fossil among branches or to be correlated among parent- echidnas (Tachyglossidae) date to no older than daughter branches. It is likely that most molecular the Middle Miocene. This disparity raises the datasets violate these assumptions (Ho et al., uncertainty of whether echidnas have a very long 2005), and the role of fossil calibrations in correct- ghost lineage or are instead derived from platypus- ing for these violations is generally underappreci- like ancestors (Musser, 2003). Recent analysis of ated. In one example, Meredith et al. (2011) show both morphological and molecular data (Phillips et that without the influence of certain calibrations, al., 2009) strongly supports the latter hypothesis, rate variation model misspecification among their and illuminates the selection of calibration bounds mammal dataset led to some groups being inferred for Monotremata. to be up to 50% too old and others >50% too The Caviomorpha-Phiomorpha and chi- young. ropteran bounds suggested here provide opportu- A further consideration is that multiple calibra- nities to more closely constrain calibrations among tions do not act as a consensus that would swamp small placental mammals. The most precise cali- any erroneous calibration information. Instead, cal- brations, and those that are typically the most infor- ibration can often be more like an auction, which mative in molecular dating analyses, tend to have can be dominated by one or a few highest (and been among large-bodied clades (e.g., Whippo- lowest) bidders, as Hallström and Janke (2010) morpha, Perissodactyla), within which parallel found for their whale-cow calibration. For this rea- slowdowns in molecular rates could bias molecular son even one set of bounds that does not include 2 PALAEO-ELECTRONICA.ORG the true divergence can substantially bias date nies are robust to character sampling error. In each estimates at other nodes, if those nodes or their case, 500 replicates were run in PAUP* 4.0b10 neighbours are not themselves closely bound. This (Swofford, 2002), with 20 random-addition heuristic provides an argument for cautious calibration. Con- searches per replicate, and characters ordered and versely, close calibration of minimum and maxi- unordered as originally specified. mum bounds lends precision to dating estimates Similar parsimony bootstrap analyses were and is important both for containing the influence of also run on a 38-taxon combined data matrix that any calibrations that are erroneous and for correct- matched the morphological data of Gunnell and ing molecular evolutionary rate models. Simmons (2005) with the 26-gene nuclear DNA With a view to balancing the competing sequences of Meredith et al. (2011) for all extant demands on calibration, there is a broad consen- chiropteran families (and outgroups Tupaia, Cyno- sus that soft bounds provide a suitable solution for cephalus, Erinaceus, Sus and Felis). The DNA maximum bounds (Parham et al., 2012; Warnock excluded the six Eocene fossil taxa, but included et al., 2012). However, there is less agreement on an additional modern pteropodid, Nyctimene. The the treatment of minimum bounds (Yang and Ran- morphological data included greater representation nala, 2006; Benton et al., 2009; Lee and Skinner, within Vespertilionidae (Antrozoini,
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