The completeness of the fossil record of mesozoic birds: implications for early avian evolution

Abstract

Many palaeobiological analyses have concluded that modern birds (Neornithes) radiated no earlier than the Maastrichtian, whereas molecular clock studies have argued for a much earlier origination. Here, we assess the quality of the fossil record of Mesozoic avian species, using a recently proposed character completeness metric which calculates the percentage of phylogenetic characters that can be scored for each taxon. Estimates of fossil record quality are plotted against geological time and compared to estimates of species level diversity, sea level, and depositional environment. Geographical controls on the avian fossil record are investigated by comparing the completeness scores of species in different continental regions and latitudinal bins. Avian fossil record quality varies greatly with peaks during the Tithonian-early Berriasian, Aptian, and Coniacian-Santonian, and troughs during the Albian-Turonian and the Maastrichtian. The completeness metric correlates more strongly with a 'sampling corrected' residual diversity curve of avian species than with the raw taxic diversity curve, suggesting that the abundance and diversity of birds might influence the probability of high quality specimens being preserved. There is no correlation between avian completeness and sea level, the number of fluviolacustrine localities or a recently constructed character completeness metric of sauropodomorph dinosaurs. Comparisons between the completeness of Mesozoic birds and sauropodomorphs suggest that small delicate vertebrate skeletons are more easily destroyed by taphonomic processes, but more easily preserved whole. Lagerstätten deposits might therefore have a stronger impact on reconstructions of diversity of smaller organisms relative to more robust forms. The relatively poor quality of the avian fossil record in the Late Cretaceous combined with very patchy regional sampling means that it is possible neornithine lineages were present throughout this interval but have not yet been sampled or are difficult to identify because of the fragmentary nature of the specimens.

Figure 1. The two opinions on the timing of modern bird origins based on molecular clocks.

A) an origin 123 million years ago during the Aptian, modified from reference ; B) an origin 135 million years ago during the Valanginian modified from reference .

Figure 2. Neornithine evolution based on a ‘literal’ interpretation of the fossil record.

According to this scenario of avian evolution, the Neornithes did not appear until the latest Cretaceous, and then diversified rapidly in the Cenozoic, whereas all basal bird groups died out at or before the K/Pg boundary. Black lines represent lineages present in the fossil record, red lines represent ghost lineages inferred from phylogenetic analysis.

Figure 3. The mean character completeness metric scores for all Mesozoic birds in each substage.

The bold blue curve represents the mean CCM2 scores, while the thin blue lines above and below it represent one standard deviation above and below the mean. Numbers of specimens are shown by the red curve to indicate sample size.

Figure 4. The CCM2 scores for Mesozoic birds, using both the complete dataset and the pruned dataset.

The complete dataset (blue curve) includes all 124 species, the pruned dataset (red curve) includes only species known to Fountaine et al .

Figure 5. Comparison of the data collected by Fountaine et al. with the CCM2.

(A) Modified from Fountaine et al.'s assessment of the completeness of the fossil record of Mesozoic birds (bird species with a completeness grade of 1 are represented by one bone, those with 2 by more than one bone, those with 3 by a nearly complete specimen, and those with 4 by more than one specimen); (B) Comparison of the mean completeness grade of bird species using the method of Fountaine et al. (red curve) and the mean CCM2 scores determined in this study (blue curve).

Figure 6. Two estimates of Mesozoic avian diversity.

(A) the raw taxic diversity estimate; (B) The residual diversity curve corrected for the number of theropod-bearing collections (dashed-dotted lines indicate standard deviation from the model).

Figure 7. A comparison of sea level and the mean CCM2 scores of Mesozoic bird specimens.

Figure 8. The mean CCM2 scores for birds found in three different palaeoenvironments: marine, fluviolacustrine, and non-fluviolactustrine terrestrial evnvironments.

Figure 9. The number of fluvialolacustrine bird-bearing localities in each substage compared to mean CCM2.

Figure 10. A comparison of the CCM2 scores of Mesozoic bird specimens and that of sauropodomorph specimens .

Figure 11. A comparison of the completeness of avian and sauropodomorph specimens.

The mean CCM2 scores of all birds (blue curve) and sauropodomorphs (red curve) in each substage from the Tithonian until the late Maastrichtian (data for Sauropodomorpha from reference [38]).

Figure 12. The number and mean CCM2 score of Mesozoic bird species found within modern latitudinal bins.

(A) The number of species found in each 5° latitudinal bin; (B) – the mean CCM2 score of all birds (blue curve) found in each latitudinal bin, with the number of specimens (red curve) to indicate sample size.

Figure 13. The geographical distribution and completeness (CCM2) of Mesozoic bird species.

(A) The number of avian species found in each landmass; (B) the mean CCM2 score of the avian species found on each landmass. Landmasses formerly part of Laurasia are represented by red bars, while those formerly part of Gondwana are represented by blue bars.

Figure 14. The mean CCM2 scores for birds assigned to the major Mesozoic avian clades.