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Short Description: Integrating the genotype and phenotype in hominid paleontology. Leslea J. Hlusko *. Department of Anthropology, 109 Davenport Hall, MC-148, 607 South Mathews ...
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Integrating the genotype and phenotype in hominid paleontology
Leslea J. Hlusko*
Department of Anthropology, 109 Davenport Hall, MC-148, 607 South Mathews Avenue, University of Illinois, Urbana, IL 61801
Communicated by Henry Harpending, University of Utah, Salt Lake City, UT, November 11, 2003
Competing interpretations of human origins and evolution have recently proliferated despite the accelerated pace of fossil discovery. These controversies parallel those involving other vertebrate families and result from the difficulty of studying evolution among closely related species. Recent advances in developmental and quantitative genetics show that some conventions routinely used by hominid and other mammalian paleontologists are unwarranted. These same advances provide ways to integrate knowledge of the genotype into the study of the phenotype. The result is an approach that promises to yield a fuller understanding of evolution below the family level.
aleontology relies on the fossil record to identify past organisms and understand many of their biological dimensions. As contemporary genetics illuminates the relationship between genotype and phenotype, the ability of fossilized anatomies to inform us about past organisms changes and expands. This is most evident in studies of large-scale organismal evolution, such as the origins of animal body plans during the Cambrian period (13), the evolution of limbs (46), and the appearance of teeth in early fishes (7). Even within more restricted groups, such as mammals, new knowledge of dental developmental genetics has elucidated evolutionary phenomenon (810). However, the significant impact that modern genetics can make on paleontological investigations at lower taxonomic levels has yet to be felt. Here, I will use human evolutionary studies to illustrate how the integration of genetics and paleontology can advance understanding. Although my examples are primate-specific, the problems within the field of human paleontology are not unique, and the methods I advocate to advance hominid studies are widely applicable across other taxa. Practical problems such as the phylogenetic proximity of taxonomic units and small and fragmentary fossil samples seriously complicate paleontological research at the subfamily level. Within hominid paleontology, these difficulties and limitations have generated three widespread, often tacit, questionable presumptions: (i) most anatomical traits are independent, (ii) most anatomical traits are adaptively informative, and (iii) small-scale morphological change is almost always parsimonious. Because some of the most contentious debates within hominid paleontology stem from these conventions, this discipline provides an appropriate example with which to illustrate how an integrated phenotypicgenotypic research approach
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promises to move us toward a better understanding of evolution below the family level. Presumption 1: Anatomical Traits Are Independent Virtually every anatomical feature on every primate bone and tooth has been named, often many times (Fig. 1; ref. 11, p. 76). Although atomization of anatomy and nomenclature has facilitated communication for centuries, many of these ``traits'' are currently used uncritically, despite the fact that this highly refined nomenclature does not necessarily translate into functionally, developmentally, or evolutionarily relevant anatomical units. Cladistics (12) is a powerful tool for reconstructing phylogenetic relationships, but it is a tool whose power is proportional to the number of independent characters available for analysis. Cladistic analyses rely on the fundamental principle that the traits analyzed are independent (1216). In human paleontology, this principle is routinely violated as functionally and developmentally linked traits are subdivided for analytical purposes. Sometimes this is because analysts are eager to squeeze the most out of the small available fragments of anatomy. Sometimes it is because the nomenclatural history of the traits themselves obfuscates the underlying biology. The continuing controversies involving hominid phylogenetics (e.g., ref. 16 vs. 17), with no clear pattern emerging from the repeated and varying analyses already undertaken, represent strong signals that a powerful method is being compromised by the input of data that do not meet the method's requirements. (For more specific critiques see refs. 1820; for counter arguments, see refs. 21 and 22. Ref. 23 highlights other problems with cladistic analyses within paleoanthropology.)
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There are direct but complex relationships between organismal anatomy and its genetic underpinnings. For example, 250 genes are known to be involved in the development of the dentition (http: bite-it.helsinki.fi). This is only a subset of all genes expressed in tooth development. Exactly what genes constitute the necessary or sufficient sets for generating various aspects of dental patterns remains unknown (24). As there may be only 30,00040,000 genes in humans (25), how should we view the 468 craniodental characters used in a recent cladistic analysis of hominids (26), or the 25 dental traits used in another (27)? Are the characters developmentally and evolutionarily independent? Based on developmental genetic studies of mice, McCollum (19) and McCollum and Sharpe (28) warn that such presumptions are questionable. Quantitative genetic and correlation studies of population variation in mice (29, 30) and primates (31) demonstrate empirically that such assumptions of independence are unfounded. Morphological integration (32), or modularity (33), is the concept that phenotypic traits will be tightly correlated when they share a common developmental pathway and or ultimate function. As such, individual morphological traits can be conceptualized as parts of sets. These sets need to be identified before their development, function, and or evolution can be studied. Olson and Miller (32), founders of this approach, studied morphological integration in the postcanine dentition of the South American monkey Aotus trivirgatus. They found differences in patterns of correlation between linear size measures of upper and lower teeth, where length and width were more strongly correlated in maxillary molars
*E-mail: hlusko@uiuc.edu. © 2004 by The National Academy of Sciences of the USA
www.pnas.org cgi doi 10.1073 pnas.0307678101
March 2, 2004
vol. 101
no. 9
26532657
