Keeping 21st Century Paleontology Grounded: Quantitative Genetic Analyses and Ancestral State Reconstruction Re-Emphasize the Essentiality of Fossils

Abstract

Advances in genetics and developmental biology are revealing the relationship between genotype and dental phenotype (G:P), providing new approaches for how paleontologists assess dental variation in the fossil record. Our aim was to understand how the method of trait definition influences the ability to reconstruct phylogenetic relationships and evolutionary history in the Cercopithecidae, the Linnaean Family of monkeys currently living in Africa and Asia. We compared the two-dimensional assessment of molar size (calculated as the mesiodistal length of the crown multiplied by the buccolingual breadth) to a trait that reflects developmental influences on molar development (the inhibitory cascade, IC) and two traits that reflect the genetic architecture of postcanine tooth size variation (defined through quantitative genetic analyses: MMC and PMM). All traits were significantly influenced by the additive effects of genes and had similarly high heritability estimates. The proportion of covariate effects was greater for two-dimensional size compared to the G:P-defined traits. IC and MMC both showed evidence of selection, suggesting that they result from the same genetic architecture. When compared to the fossil record, Ancestral State Reconstruction using extant taxa consistently underestimated MMC and PMM values, highlighting the necessity of fossil data for understanding evolutionary patterns in these traits. Given that G:P-defined dental traits may provide insight to biological mechanisms that reach far beyond the dentition, this new approach to fossil morphology has the potential to open an entirely new window onto extinct paleobiologies. Without the fossil record, we would not be able to grasp the full range of variation in those biological mechanisms that have existed throughout evolution.

Keywords: Cercopithecidae; dentition; evolution; genotype:phenotype mapping; monkeys; phylogeny; primates.

Figure 1

Illustration of the four maxillary dental traits investigated in this analysis. Each panel shows the right maxillary occlusal view of two extremes for one of the traits. Mesial is to the top, distal to the bottom, lingual to the right, and buccal to the left. The axis at the bottom of the figure orients the reader to how the morphology varies according to low and high values of the trait. (Panels (A,B)) demonstrate the two traits defined through quantitative genetic analyses, ratios that reflect the relative size variation between the premolar and molar genetic modules (PMM; panel (A)) and the relative sizes of the molars within the molar module (MMC; panel (B)). (Panel (C)) shows the traditional method for studying molar size variation within paleontology, by calculating a two-dimensional area of the occlusal view of the crown. (Panel (D)) shows the “inhibitory cascade” (IC) trait, defined through developmental gene expression studies of mice. See text for more detailed descriptions.

Figure 2

Molecular phylogeny of the extant cercopithecid genera included in this analysis with ASR nodes indicated. See Table 8 for ASR MMC and ASR PMM estimates.

Figure 3

Box and whisker plots showing the range of variation for PMM and MMC within the sampled extant genera (labeled at the bottom of the figure). The genera are color-coded, with tribe Cercopithecini in gold, tribe Papionini in blue, and the subfamily Colobinae in purple. In addition to the extant data, we plot trait estimates for the Ancestral State Reconstruction (ASR) nodes as horizontal dotted lines, labeled with N and the number of the node. The possible fossil representatives for these nodes are plotted within the tribe or subfamily to which the fossil belongs. Victoriapithecus, on the far left, is widely thought to be ancestral to the split between the Colobinae and the Cercopithecinae (which includes Cercopoithecini and Papionini, shown here) [99]. Notice that for all but two of the PMM ASR-fossil pairs, the ASR estimate is lower than the observed fossil values. Similarly, for all but two of the MMC ASR-fossil pairs, the ASR estimate is also lower than the observed values. These differences are shown quantitatively in Figure 4.

Figure 4

Bivariate plot of the difference between ASR trait values and fossil evidence for PMM and MMC. Geological age is shown on the X-axis. On the Y-axis, we report the absolute value of the difference between the ASR-estimated trait value for each node (molecular divergence) and the trait values observed for the African cercopithecid fossil genera in the same Tribe living near the time of the molecular divergence. The genera are shown in separate colors, defined in the key to the right. Triangles represent the PMM trait, and circles represent the MMC trait. The average difference for PMM is indicated by the top dashed line. The average difference for MMC is indicated by the lower dashed line. Procercocebus and Soromandrillus are included twice, as they could represent the ancestral morphology for nodes 28, 29, and 30.