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The integration of quantitative genetics, paleontology, and neontology reveals genetic underpinnings of primate dental evolution - PubMed

  • ️Fri Jan 01 2016

The integration of quantitative genetics, paleontology, and neontology reveals genetic underpinnings of primate dental evolution

Leslea J Hlusko et al. Proc Natl Acad Sci U S A. 2016.

Abstract

Developmental genetics research on mice provides a relatively sound understanding of the genes necessary and sufficient to make mammalian teeth. However, mouse dentitions are highly derived compared with human dentitions, complicating the application of these insights to human biology. We used quantitative genetic analyses of data from living nonhuman primates and extensive osteological and paleontological collections to refine our assessment of dental phenotypes so that they better represent how the underlying genetic mechanisms actually influence anatomical variation. We identify ratios that better characterize the output of two dental genetic patterning mechanisms for primate dentitions. These two newly defined phenotypes are heritable with no measurable pleiotropic effects. When we consider how these two phenotypes vary across neontological and paleontological datasets, we find that the major Middle Miocene taxonomic shift in primate diversity is characterized by a shift in these two genetic outputs. Our results build on the mouse model by combining quantitative genetics and paleontology, and thereby elucidate how genetic mechanisms likely underlie major events in primate evolution.

Keywords: dental variation; neontology; paleontology; primates; quantitative genetics.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Mandibular MMC and PMM for extant and fossil OWMs. (A) We show the log of mandibular P4 versus M1 areas for extant taxa, a common means through which to describe and assess dental variation in extant and extinct OWMs. We provide this log as a comparison with the next panel. (B) We plot the MMC and PMM for extant cercopithecoids, demonstrating how well these two phenotypes separate the various taxa in comparison to the more traditional method shown in A. The red dot in the center represents where the sister taxon, Victoriapithecidae, plots relative to the extant species. (C) We have plotted the mean for each extant species as a single dot, using the same color coding as in the previous panels. On top of this plotted mean, we plot fossil data from Africa with letter designations, defined to the right of the graph. Colobine fossil taxa are illustrated in green, papionin fossil taxa in blue, and Victoriapithecus in red. Nodes that link taxa are shown in black. More comparisons are provided in SI Appendix, Fig. S2.

Fig. 2.
Fig. 2.

Mandibular MMC and PMM for extant hominoids and fossil hominids. (A) We plot individual points for the extant hominoid taxa. Notice that, as we found for the OWMs, these two phenotypes separate the genera and species quite well. (B) We show the mean for each extant hominoid species as a single dot, using the same color coding as in the previous panel. On top of this mean, we plot hominid fossil data with letter designations, save for the genus Homo, which is shown using shapes. Abbreviations are as follows: Au. afa, Australopithecus afarensis; Au. afr, Australopithecus africanus; Au. anam, Australopithecus anamensis; Au. boi, Australopithecus boisei; Au. gar, Australopithecus garhi; Ar. ram, Ardipithecus ramidus; Au. rob, Australopithecus robustus. (C) We combine the extant data for OWMs (as seen in Fig. 1C) and hominoids (as seen in Fig. 2B) with fossil data for Miocene apes (using abbreviations). The fossils are color-coded by age: Early Miocene is shown in brown, Middle Miocene in gray, and Late Miocene in black. The fossil hominoids in the upper MMC range only date to the early part of the Miocene, and by the Plio-Pleistocene, this primate morphospace is occupied exclusively by the papionins (in purple and blue). Extant hominoids occupy only the lowest range of the MMC, far below the morphospace of the Miocene apes, but remain in the same PMM range (compare with B).

Fig. 3.
Fig. 3.

Overview of climate change, primate phylogeny, and primate taxonomic diversity compared with the evolution of the MMC and PMM. (A) Global deep-sea oxygen and carbon isotope records, adapted from a study by Zachos et al. (34). Higher δ18O values indicate cooler temperatures. The δ13C values represent different flora. (B) Our disparity through time results, which are discussed in the main text. Dotted lines indicate the predicted disparity values, and shaded areas indicate their 95% CIs. Solid lines indicate actual trait values. Values near 0 indicate that a particular clade contains little of the overall variation, and that variation in the trait is partitioned between subclades rather than within them. Values near 1.0 suggest that a clade contains a large amount of that variation, and that clades may overlap in trait space. For the PMM and MMC, trait values fall significantly below expected values beginning in the Middle Miocene, indicating trait partitioning between subfamilies within primates. Disparity through time plots of other phenotypes are provided in SI Appendix, Fig. S4. (C) Phylogeny of extant primates based on molecular data. (D) Anthropoid taxonomic diversity through time. Oligocene counts are not included because they precede the cercopithecoid–hominoid split.

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