Completeness of the eutherian mammal fossil record and implications for reconstructing mammal evolution through the Cretaceous/Paleogene mass extinction

Abstract

There is a well-established discrepancy between paleontological and molecular data regarding the timing of the origin and diversification of placental mammals. Molecular estimates place interordinal diversification dates in the Cretaceous, while no unambiguous crown placental fossils have been found prior to the end-Cretaceous mass extinction. Here, the completeness of the eutherian fossil record through geological time is evaluated to assess the suggestion that a poor fossil record is largely responsible for the difference in estimates of placental origins. The completeness of fossil specimens was measured using the character completeness metric, which quantifies the completeness of fossil taxa as the percentage of phylogenetic characters available to be scored for any given taxon. Our data set comprised 33 published cladistic matrices representing 445 genera, of which 333 were coded at the species level.There was no significant difference in eutherian completeness across the Cretaceous/Paleogene (K/Pg) boundary. This suggests that the lack of placental mammal fossils in the Cretaceous is not due to a poor fossil record but more likely represents a genuine absence of placental mammals in the Cretaceous. This result supports the “explosive model” of early placental evolution, whereby placental mammals originated around the time of the K/Pg boundary and diversified soon after.No correlation was found between the completeness pattern observed in this study and those of previous completeness studies on birds and sauropodomorph dinosaurs, suggesting that different factors affect the preservation of these groups. No correlations were found with various isotope proxy measures, but Akaike information criterion analysis found that eutherian character completeness metric scores were best explained by models involving the marine-carbonate strontium-isotope ratios (87Sr/86Sr), suggesting that tectonic activity might play a role in controlling the completeness of the eutherian fossil record.

Rapid morphological evolution in placental mammals post-dates the origin of the crown group

“…R. Soc. B 286: 20182418 [20,21] such that we should expect to have found Cretaceous placentals if they did exist, although Foote et al [20, p. 1312] note three hypotheses that could explain the discrepancy between their results and postulated missing evolutionary history of eutherian mammals. Their first hypothesis posits that 'Cretaceous members of the modern eutherian orders are preserved and described, but they are not recognized because they are so primitive and lack most diagnostic features', with the prediction that 'both morphological evolution be largely decoupled from lineage splitting and molecular evolution and that eutherians experienced much lower rates of morphological change through the Cretaceous than during the Cenozoic'.…”

“…Moreover, sampling of Northern Hemisphere localities is sufficiently dense that we would expect to have found Cretaceous placentals were they to have existed there [20]. Available fossils are of equal quality (in terms of scorable phylogenetically informative characters) in the Cretaceous as in the earliest Paleocene [21]. The only remaining hiding places for an 'off-camera' diversification of placental mammals are within unpreserved environments in the Northern Hemisphere; some environments are not conducive to fossilization [22].…”

Quantifying the completeness of the bat fossil record

“…), plesiosaurs (Tutin & Butler ) and Cretaceous and Palaeogene eutherian mammals (Davies et al . ). Mannion & Upchurch () presented their sauropodomorph data in substage time bins, but this was recalculated into stage‐level time bins by Dean et al .…”

“…; Davies et al . ). These studies aim to assess variation in information content of fossil taxa and the entire record of a group, rather than trying to quantify temporal gaps in the record or stratigraphic fit.…”

Diversity and dispersal trends following the latest-permian mass extinction

“…These mass extinctions sometimes mark the demise of previously dominant groups of organisms, and create the conditions in which new groups can achieve evolutionary success; terrestrial examples include the demise of therapsids and the ensuing rise of archosaurs following the latest-Permian mass extinction (Nicolas and Rubidge, 2010;Ezcurra and Butler, 2018), the replacement of several pseudosuchian clades with dinosaurs following the Tr-J extinction (Brusatte et al, 2008a(Brusatte et al, , 2010, and the radiation of mammals following the loss of non-avian dinosaur diversity during the K-Pg mass extinction (Clemens, 2010;Davies et al, 2017).…”