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. 2019 Mar 13;286(1898):20182418.
doi: 10.1098/rspb.2018.2418.

Rapid Morphological Evolution in Placental Mammals Post-Dates the Origin of the Crown Group

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Free PMC article

Rapid Morphological Evolution in Placental Mammals Post-Dates the Origin of the Crown Group

Thomas J D Halliday et al. Proc Biol Sci. .
Free PMC article

Abstract

Resolving the timing and pattern of early placental mammal evolution has been confounded by conflict among divergence date estimates from interpretation of the fossil record and from molecular-clock dating studies. Despite both fossil occurrences and molecular sequences favouring a Cretaceous origin for Placentalia, no unambiguous Cretaceous placental mammal has been discovered. Investigating the differing patterns of evolution in morphological and molecular data reveals a possible explanation for this conflict. Here, we quantified the relationship between morphological and molecular rates of evolution. We show that, independent of divergence dates, morphological rates of evolution were slow relative to molecular evolution during the initial divergence of Placentalia, but substantially increased during the origination of the extant orders. The rapid radiation of placentals into a highly morphologically disparate Cenozoic fauna is thus not associated with the origin of Placentalia, but post-dates superordinal origins. These findings predict that early members of major placental groups may not be easily distinguishable from one another or from stem eutherians on the basis of skeleto-dental morphology. This result supports a Late Cretaceous origin of crown placentals with an ordinal-level adaptive radiation in the early Paleocene, with the high relative rate permitting rapid anatomical change without requiring unreasonably fast molecular evolutionary rates. The lack of definitive Cretaceous placental mammals may be a result of morphological similarity among stem and early crown eutherians, providing an avenue for reconciling the fossil record with molecular divergence estimates for Placentalia.

Keywords: Placentalia; evolution; molecular clock; morphology; palaeontology; rate.

Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Majority rule consensus tree of all maximum-likelihood topologies generated across the 1000 replicates for 57 extant and 191 extinct therian taxa. Node annotations are internode certainties across all conflicting bipartitions (the ICA of Salichos et al. [50]). Support for most divisions within Placentalia is generally poor.
Figure 2.
Figure 2.
The phylogeny of extant placentals. (a) Topology of extant placentals indicating branches with high (red) or low (blue) ratios of morphological : molecular evolution. Node numbers indicate clades; as follows: 1, Placentalia; 2, Atlantogenata; 3, Boreoeutheria; 4, Xenarthra; 5, Afrotheria; 6, Laurasiatheria; 7, Euarchontoglires; 8, Eulipotyphla; 9, Scrotifera; 10, Chiroptera; 11, Artiodactyla; 12, Pegasoferae; 13, Perissodactyla; 14, Carnivora; 15, Glires; 16, Lagomorpha; 17, Rodentia; 18, Euarchonta; 19, Scandentia; 20, Primates. (b) Averaged molecular partition branch lengths. (c) Averaged morphological partition branch lengths.
Figure 3.
Figure 3.
Rates of morphological and molecular evolution through time. (a) Relative rate of morphological and molecular evolution through time according to four major dating hypotheses for placental mammal nodes, as follows: (i) Halliday and Goswami 2016, derived from a stochastic model and fossil occurrence data [10], (ii) Phillips 2016, derived from molecular data and incorporating strong assumptions about fossil calibrations [15], (iii) Meredith et al. 2011, a maximum likelihood relaxed clock model [13], and (iv) dos Reis et al. 2012, dated using a Bayesian approach and phylogenomic dataset [12]. Although molecular-derived dates still imply an increase in morphological evolution prior to the end-Cretaceous mass extinction, the fact that this is not associated with the origin of Placentalia substantially reduces the conflict between the observations from fossil data and molecular-derived dates. Curves are presented excluding Xenarthra, because the exceptionally high rate ratios leading to that node overwhelm the signal from other branches of the phylogeny; versions including Xenarthra are available as the electronic supplementary material, figure 1A–D. (b) Absolute morphological (dotted line) and molecular (dashed line) rates of evolution through time for the four timetrees. In all but that of Halliday et al. [10], estimated absolute molecular rates undergo few major shifts over time. We note that even in the Halliday et al. [10] timetree, which has the shortest branch durations, molecular rates are not excessively high near the K-Pg boundary. All molecular-derived trees imply some degree of morphological diversification during the Cretaceous that has not been observed, although the Cretaceous spike in the Phillips [15] tree represents the origin of Xenarthra, expected to have occurred in the undersampled southern continents.

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