Genetic integration of molar cusp size variation in baboons

Many studies of primate diversity and evolution rely on dental morphology for insight into diet, behavior, and phylogenetic relationships. Consequently, variation in molar cusp size has increasingly become a phenotype of interest. In 2007 we published a quantitative genetic analysis of mandibular molar cusp size variation in baboons. Those results provided more questions than answers, as the pattern of genetic integration did not fit predictions from odontogenesis. To follow up, we expanded our study to include data from the maxillary molar cusps. Here we report on these later analyses, as well as inter‐arch comparisons with the mandibular data. We analyzed variation in two‐dimensional maxillary molar cusp size using data collected from a captive pedigreed breeding colony of baboons, Papio hamadryas, housed at the Southwest National Primate Research Center. These analyses show that variation in maxillary molar cusp size is heritable and sexually dimorphic. We also estimated additive genetic correlations between cusps on the same crown, homologous cusps along the tooth row, and maxillary and mandibular cusps. The pattern for maxillary molars yields genetic correlations of one between the paracone–metacone and protocone–hypocone. Bivariate analyses of cuspal homologues on adjacent teeth yield correlations that are high or not significantly different from one. Between dental arcades, the nonoccluding cusps consistently yield high genetic correlations, especially the metaconid–paracone and metaconid–metacone. This pattern of genetic correlation does not immediately accord with the pattern of development and/or calcification, however these results do follow predictions that can be made from the evolutionary history of the tribosphenic molar. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Evolution of genetically correlated traits: tooth size and body size in baboons

Within a population, only phenotypic variation that is influenced by genes will respond to selection. Genes with pleiotropic effects are known to influence numerous traits, complicating our understanding of their evolution through time. Here we use quantitative genetic analyses to identify and estimate the shared genetic effects between molar size and trunk length in a pedigreed, breeding population of baboons housed at the Southwest National Primate Research Center. While crown area has a genetic correlation with trunk length, specific linear measurements yield different results. We find that variation in molar buccolingual width and trunk length is influenced by overlapping additive genetic effects. In contrast, mesiodistal molar length appears to be genetically independent of body size. This is the first study to demonstrate a significant genetic correlation between tooth size and body size in primates. The evolutionary implications are discussed.     

Statistical genetics of molar cusp patterning in pedigreed baboons: implications for primate dental development and evolution

Gene expression and knock-out studies provide considerable information about the genetic mechanisms required for tooth organogenesis. Quantitative genetic studies of normal phenotypic variation are complementary to these developmental studies and may help elucidate the genes and mechanisms that contribute to the normal population-level phenotypic variation upon which selection acts. Here we present the first quantitative genetic analysis of molar cusp positioning in mammals. We analyzed quantitative measures of molar cusp position in a captive pedigreed baboon breeding colony housed at the Southwest National Primate Research Center in San Antonio, Texas. Our results reveal complete pleiotropy between antimeric pairs of traits--i.e., they are influenced by the same gene or suite of genes. Mandibular morphological homologues in the molar series also exhibit complete pleiotropy. In contrast, morphological homologues in maxillary molar series appear to be influenced by partial, incomplete pleiotropic effects. Variation in the mandibular mesial and distal molar loph orientation on the same molar crown is estimated to be genetically independent, whereas the maxillary molar mesial and distal loph orientation is estimated to have partially overlapping genetic affects. The differences between the maxillary and mandibular molar patterning, and the degree of genetic independence found between lophs on the same molar crown, may be indicative of previously unrecognized levels of modularity in the primate dentition.     

Modularity in the mammalian dentition: mice and monkeys share a common dental genetic architecture

The concept of modularity provides a useful tool for exploring the relationship between genotype and phenotype. Here, we use quantitative genetics to identify modularity within the mammalian dentition, connecting the genetics of organogenesis to the genetics of population-level variation for a phenotype well represented in the fossil record. We estimated the correlations between dental traits owing to the shared additive effects of genes (pleiotropy) and compared the pleiotropic relationships among homologous traits in two evolutionary distant taxa-mice and baboons. We find that in both mice and baboons, who shared a common ancestor >65 Ma, incisor size variation is genetically independent of molar size variation. Furthermore, baboon premolars show independent genetic variation from incisors, suggesting that a modular genetic architecture separates incisors from these posterior teeth as well. Such genetic independence between modules provides an explanation for the extensive diversity of incisor size variation seen throughout mammalian evolution-variation uncorrelated with equivalent levels of postcanine tooth size variation. The modularity identified here is supported by the odontogenic homeobox code proposed for the patterning of the rodent dentition. The baboon postcanine pattern of incomplete pleiotropy is also consistent with predictions from the morphogenetic field model.     

The relation of canine size to pattern and extent of attrition in baboons

For most genera of animals the association between dental morphology and diet is such that inferences concerning the diet can be made on the basis of the dentition alone. The canine is the one tooth that appears exempt from such generalisation and exhibits a wide range of variability of size and shape in all groups. In order to determine the effect of dimorphism of the canine on the dental apparatus, male and female specimens of Theropithecus and Papio baboons were examined. Occlusal relationships and dental pathology for 21 Theropithecus and 40 Papio skulls were recorded, and crown height measurements obtained for maxillary incisors, buccal and lingual molar cusps. Attrition was the most common and severe cause of abscess formation in older animals: the pattern of attrition differed in adult males and females, the latter showing more wear of the incisor and lingual molar cusps. Partial correlations for incisor, buccal and lingual molar cuspal crown height show a significant correlation between incisor and lingual cusp attrition in juveniles of both sexes and adult females (p < 0.01). Adult males show no correlation of attrition. It is proposed that the correlation of incisor and lingual molar cusp attrition is associated with anterior-posterior grinding movements, such as take place during incision, that the large canine present in the male limits such movements, the sharp blade-like canine being employed as a cutting tool. This use of the canine by reducing functional demands on other teeth, prolongs the utility of the dental apparatus, and hence the lifespan of its possessor.     

Associations between Carabelli trait and cusp areas in human permanent maxillary first molars

Few dental anthropological studies have investigated the associations between tooth crown size and crown traits in humans using quantitative methods. We tested several hypotheses about overall crown size, individual cusp areas, and expression of Carabelli cusps in human permanent first molars by obtaining data from standardized occlusal photographs of 308 Australians of European descent (171 males and 137 females). Specifically, we aimed to calculate the areas of the four main molar cusps, and also Carabelli cusp, and to compare the relative variability of cusp areas in relation to timing of development. We also aimed to compare cusp areas between males and females and to describe how Carabelli cusp interacted with other molar cusps. Measurements included maximum crown diameters (mesiodistal and buccolingual crown diameters), the areas of the four main cusps, and the area of Carabelli cusp. The pattern of relative variability in absolute areas of molar cusps corresponded with their order of formation, the first-forming paracone displaying the least variation, and the last-forming Carabelli cusp showing the greatest. Overall crown size and areas of individual cusps all showed sexual dimorphism, with values in males exceeding those in females. Sexual dimorphism was smallest for paracone area and greatest for Carabelli cusp area. Overall crown size and cusp areas were larger in individuals displaying a Carabelli cusp, especially the hypocone area. Although the combined area of the protocone and a Carabelli cusp was greater in cuspal forms than noncuspal forms, protocone area alone was significantly smaller in the former. Our findings lead us to propose that, in individuals with the genotype for Carabelli trait expression, larger molar crowns are more likely to display Carabelli cusps, whereas molars with smaller crowns are more likely to display reduced forms of expression of the trait. We suggest that the pattern of folding of the internal enamel epithelium in developing molar crowns, particularly in the protocone region, can be modified by a developing Carabelli cusp.     

A COMPARATIVE ANALYSIS OF MORPHOLOGICAL VARIATION PATTERNS IN THE PAPIONINS

Comparative studies of intraspecific variation patterns are important in attempts to reconstruct the differential selection pressures experienced by related species and in assessing the resultant observed interspecific variation. Reconstruction of past selection depends on an assumption of relatively stable patterns of genetic variance and covariance through time and across related species. Models by Lande (1979) and Turelli (1988a, 1988b) lead to contrasting expectations of stability versus lability of variation patterns, respectively, at least for closely related species. I report on a comparative study of phenotypic variance and correlation patterns in seven species of papionins, including macaques, baboons, and mangabeys, in order to determine the stability of variation patterns in this group. The three-dimensional coordinates of 12 bony landmarks on the face were used in a finite-element scaling analysis in order to measure local size variation at each landmark. Variances and correlations for these local size metrics were calculated using pooled sex-specific values. Variation patterns were compared across species using vector and matrix correlations in combination with various randomization-based significance tests. Patterns of variation and correlation were generally quite similar across the seven species, although some differences were also apparent. The overall magnitude of correlation is also similar among species, as only a few interspecific comparisons showed significant differences. Thus, it is concluded that patterns of variation and correlation in facial morphology have tended to remain stable in this group of primates. This result should allow for reconstruction of past differential selection pressures in the clade. The pattern of similarity among correlation structures for these species showed no association with their phylogenetic relationships.     

Genetic variation in pathogen-induced early hatching of toad embryos

Accelerated hatching is one of few defences available to embryos, and is effective against many egg-stage risks. We present the first analysis of genetic variation in hatching plasticity, examining premature hatching of American toad embryos in response to pathogenic water moulds. We reared eggs from half- and full-sib families in the presence and absence of water mould. Hatching age and hatchling size showed low cross-environment genetic correlations, suggesting that early-induced hatching can evolve largely independently of spontaneous hatching. We found less phenotypic and additive genetic variation for early-induced hatching than spontaneous hatching, and a stronger correlation between egg and induced hatchling sizes. Directional selection by the pathogen may have eroded variation in early-induced hatching, pushing it against the constraint of hatching gland development. Later hatching has a second, muscular component. This pattern of variation may characterize defences based on developmental transitions, although other inducible defences show more variation in induced phenotypes.     

Intercusp relationships of the permanent maxillary first and second molars in American whites

Much of a human molar's morphology is concentrated on its occlusal surface. In view of embryologists' recent attention on the determination of crown morphology by enamel knots that initiate cusp formation, we were interested in the arrangement of cusp apices in the definitive tooth. Computer-assisted image analysis was used to measure intercusp distances and angles on permanent maxillary M1 and M2 in a sample of 160 contemporary North American whites. The intent was to generate normative data and to compare the size and variability gradients from M1 to M2. There is little sexual dimorphism in intercusp distances or angles, even though the conventional mesiodistal (MD) and buccolingual (BL) crown size is 2.0% and 4.0% larger in males, respectively, in these same teeth. Dimensions decreased in size and increased in variability from M1 to M2, but differentially. Cusps of the trigon were more stable between teeth, especially the paracone-protocone relationship. Principal components analysis on the six M1 distances disclosed only one eigenvalue above 1.0, indicating that overall crown size itself is the paramount controlling factor in this tooth that almost invariably exhibits a hypocone. In contrast, four components were extracted from among the 12 angular cusp relationships in M1. These axes of variation may prove useful in studies of intergroup differences. A shape difference occurs in M2, depending on whether the hypocone is present; when absent, the metacone is moved lingually, creating more of an isosceles arrangement for the cusps of the trigon. Statistically, correlations are low between occlusal intercusp relationships and conventional crown diameters measured at the margins of the crowns that form later. Weak statistical dependence between cusp relationships and traditional MD and BL diameters suggest that separate stage- and location-specific molecular signals control these different parts (and different stages) of crown formation.     

Quantitative Genetics,Pleiotropy, and Morphological Integration in the Dentition of <Emphasis Type="Italic">Papio hamadryas</Emphasis>

Variation in the mammalian dentition is highly informative of adaptations and evolutionary relationships, and consequently has been the focus of considerable research. Much of the current research exploring the genetic underpinnings of dental variation can trace its roots to Olson and Miller’s 1958 book Morphological Integration. These authors explored patterns of correlation in the post-canine dentitions of the owl monkey and Hyopsodus, an extinct condylarth from the Eocene. Their results were difficult to interpret, as was even noted by the authors, due to a lack of genetic information through which to view the patterns of correlation. Following in the spirit of Olson and Miller’s research, we present a quantitative genetic analysis of dental variation in a pedigreed population of baboons. We identify patterns of genetic correlations that provide insight to the genetic architecture of the baboon dentition. This genetic architecture indicates the presence of at least three modules: an incisor module that is genetically independent of the post-canine dentition, and a premolar module that demonstrates incomplete pleiotropy with the molar module. We then compare this matrix of genetic correlations to matrices of phenotypic correlations between the same measurements made on museum specimens of another baboon subspecies and the Southeast Asian colobine Presbytis. We observe moderate significant correlations between the matrices from these three primate taxa. From these observations we infer similarity in modularity and hypothesize a common pattern of genetic integration across the dental arcade in the Cercopithecoidea.     

Evolution of floral display in Eichhornia paniculata (Pontederiaceae): direct and correlated responses to selection on flower size and number

Trade-offs between flower size and number seem likely to influence the evolution of floral display and are an important assumption of several theoretical models. We assessed floral trade-offs by imposing two generations of selection on flower size and number in a greenhouse population of bee-pollinated Eichhornia paniculata. We established a control line and two replicate selection lines of 100 plants each for large flowers (S+), small flowers (S-), and many flowers per inflorescence (N+). We compared realized heritabilities and genetic correlations with estimates based on restricted-maximum-likelihood (REML) analysis of pedigrees. Responses to selection confirmed REML heritability estimates (flower size, h2 = 0.48; daily flower number, h2 = 0.10; total flower number, h2 = 0.23). Differences in nectar, pollen, and ovule production between S+ and S- lines supported an overall divergence in investment per flower. Both realized and REML estimates of the genetic correlation between daily and total flower number were r = 1.0. However, correlated responses to selection were inconsistent in their support of a trade-off. In both S- lines, correlated increases in flower number indicated a genetic correlation of r = -0.6 between flower size and number. In contrast, correlated responses in N+ and S+ lines were not significant, although flower size decreased in one N+ line. In addition, REML estimates of genetic correlations between flower size and number were positive, and did not differ from zero when variation in leaf area and age at first flowering were taken into account. These results likely reflect the combined effects of variation in genes controlling the resources available for flowering and genes with opposing effects on flower size and number. Our results suggest that the short-term evolution of floral display is not necessarily constrained by trade-offs between flower size and number, as is often assumed.     

Genetic, geographic, and environmental correlates of human temporal bone variation

Temporal bone shape has been shown to reflect molecular phylogenetic relationships among hominoids and offers significant morphological detail for distinguishing taxa. Although it is generally accepted that temporal bone shape, like other aspects of morphology, has an underlying genetic component, the relative influence of genetic and environmental factors is unclear. To determine the impact of genetic differentiation and environmental variation on temporal bone morphology, we used three-dimensional geometric morphometric techniques to evaluate temporal bone variation in 11 modern human populations. Population differences were investigated by discriminant function analysis, and the strength of the relationships between morphology, neutral molecular distance, geographic distribution, and environmental variables were assessed by matrix correlation comparisons. Significant differences were found in temporal bone shape among all populations, and classification rates using cross-validation were relatively high. Comparisons of morphological distances to molecular distances based on short tandem repeats (STRs) revealed a significant correlation between temporal bone shape and neutral molecular distance among Old World populations, but not when Native Americans were included. Further analyses suggested a similar pattern for morphological variation and geographic distribution. No significant correlations were found between temporal bone shape and environmental variables: temperature, annual rainfall, latitude, or altitude. Significant correlations were found between temporal bone size and both temperature and latitude, presumably reflecting Bergmann's rule. Thus, temporal bone morphology appears to partially follow an isolation by distance model of evolution among human populations, although levels of correlation show that a substantial component of variation is unexplained by factors considered here.     

DEVELOPMENT,FUNCTION, AND THE QUANTITATIVE GENETICS OF WING MELANIN PATTERN IN PIERIS BUTTERFLIES

Do genetic correlations among phenotypic characters reflect developmental organization or functional coadaptation of the characters? We test these hypotheses for the wing melanin pattern of Pieris occidentalis butterflies, by comparing estimated genetic correlations among wing melanin characters with a priori predictions of the developmental organization and the functional (thermoregulatory) organization of melanin pattern. There were significant broad-sense heritabilities and significant genetic correlations for most melanin characters. Matrix correlation tests revealed significant agreement between the observed genetic correlations and both developmental and functional predictions in most cases; this occurred even when the overlap between developmental and functional predictions was eliminated. These results suggest that both developmental organization and functional coadaptation among melanin characters influence the genetic correlation structure of melanin pattern in this species. These results have two important implications for the evolution of melanin pattern in P. occidentalis and other butterflies: 1) most phenotypic variation in pattern may reflect variation among, rather than within, sets of developmentally homologous wing melanin characters; and 2) in a changing selective environment, genetic correlations may retard the disruption of functionally coupled melanin characters, thus affecting the evolutionary response to selection.     

The dentinoenamel junction in primates

Dental characteristics figure large in primate taxonomy because teeth fossilize commonly and reflect dietary adaptations. The mammalian dentinoenamel junction (DEJ) plays a crucial role throughout odontogenesis in determining the ultimate crown configuration, being the interface between the papilla and the dental cap. The final configuration of the dentin surface reflects the epithelium more closely than does the enamel surface of the crown. Enamel deposition occurs relatively late in calcification, often causing many changes from the pattern residing in the DEJ; the genetic determination of the two surfaces also differs. Comparative study of the DEJ (and its differences from the enamel crown) is a potential adjunct to dentition-based taxonomy and may help to resolve certain cusp homologies and morphogenetic order of appearance. Primate teeth were stripped of enamel after measurement, mapping, and anatomical observations on the original crown. The dentin surfaces thus revealed differ from the enamel surfaces in several respects and shed new light on such dental problem areas as the origin of the hypocone, the affinities of lorisoids and callitrichids, the monophyly of the anthropoid grade, and human affinities.     

A genomewide linkage scan for quantitative trait loci influencing the craniofacial complex in baboons (Papio hamadryas spp.)

Numerous studies have detected significant contributions of genes to variation in development, size, and shape of craniofacial traits in a number of vertebrate taxa. This study examines 43 quantitative traits derived from lateral cephalographs of 830 baboons (Papio hamadryas) from the pedigreed population housed at the Southwest National Primate Research Center. Quantitative genetic analyses were conducted using the SOLAR analytic platform, a maximum-likelihood variance components method that incorporates all familial information for parameter estimation. Heritability estimates were significant and of moderate to high magnitude for all craniofacial traits. Additionally, 14 significant quantitative trait loci (QTL) were identified for 12 traits from the three developmental components (basicranium, splanchnocranium, and neurocranium) of the craniofacial complex. These QTL were found on baboon chromosomes (and human orthologs) PHA1 (HSA1), PHA 2 (HSA3), PHA4 (HSA6), PHA11 (HSA12), PHA13 (HSA2), PHA16 (HSA17), and PHA17 (HSA13) (PHA, P. hamadryas; HSA, Homo sapiens). This study of the genetic architecture of the craniofacial complex in baboons provides the groundwork needed to establish the baboon as an animal model for the study of genetic and nongenetic influences on craniofacial variation.     

Heritability of resting metabolic rate in a wild population of blue tits

We report the first study with the aim to estimate heritability in a wild population, a nest box breeding population of blue tits. We estimated heritability as well as genetic and phenotypic correlations of resting metabolic rate (RMR), body mass and tarsus length with an animal model based on data from a split cross‐fostering experiment with brood size manipulations. RMR and body mass, but not tarsus length, showed significant levels of explained variation but for different underlying reasons. In body mass, the contribution to the explained variation is mainly because of a strong brood effect, while in RMR it is mainly because of a high heritability. The additive variance in RMR was significant and the heritability was estimated to 0.59. The estimates of heritability of body mass (0.08) and tarsus length (0.00) were both low and based on nonsignificant additive variances. Thus, given the low heritability (and additive variances) in body mass and tarsus length the potential for direct selection on RMR independent of the two traits is high in this population. However, the strong phenotypic correlation between RMR and mass (0.643 ± 0.079) was partly accounted for by a potentially strong, although highly uncertain, genetic correlation (1.178 ± 0.456) between the two traits. This indicates that the additive variance of body mass, although low, might still somewhat constrain the independent evolvability of RMR.     

Intraspecific variation in sex allocation in hermaphroditic Plantago coronopus (L.)

Models for sex allocation assume that increased expenditure of resources on male function decreases the resources available for female function. Under some circumstances, a negative genetic correlation between investment in stamens and investment in ovules or seeds is expected. Moreover, if fitness returns for investment in male and female function are different with respect to size, sex allocation theory predicts size‐specific gender changes. We studied sex allocation and genetic variation for investment in stamens, ovules and seeds at both the flower and the plant level in a Dutch population of the wind‐pollinated and predominantly outcrossing Plantago coronopus. Data on biomass of floral structures, stamens, ovules, seedset and seedweight were used to calculate the average proportion of reproductive allocation invested in male function. Genetic variation and (genetic) correlations were estimated from the greenhouse‐grown progeny of maternal families, raised at two nutrient levels. The proportion of reproductive biomass invested in male function was high at flowering (0.86 at both nutrient levels) and much lower at fruiting (0.30 and 0.40 for the high and low nutrient treatment, respectively). Androecium and gynoecium mass exhibited moderately high levels of genetic variance, with broad‐sense heritabilities varying from 0.35 to 0.56. For seedweight no genetic variation was detected. Significant among‐family variation was also detected for the proportion of resources invested in male function at flowering, but not at fruiting. Phenotypic and broad‐sense genetic correlations between androecium and gynoecium mass were positive. Even after adjusting for plant size, as a measure of resource acquisition, maternal families that invested more biomass in the androecium also invested more in the gynoecium. This is consistent with the hypothesis that genetic variation for resource acquisition may in part be responsible for the overall lack of a negative correlation between male and female function. Larger plants had a more female‐biased allocation pattern, brought about by an increase in seedset and seedweight, whereas stamen biomass did not differ between small and large plants. These results are discussed in relation to size‐dependent sex allocation theory (SDS). Our results indicate that the studied population harboured substantial genetic variation for reproductive characters.     

Microsatellite Variation in Two Populations of Free-Ranging Yellow Baboons (Papio hamadryas cynocephalus)

We investigated genetic variation at six microsatellite (simple sequence repeat) loci in yellow baboons (Papio hamadryas cynocephalus) at two localities: the Tana River Primate Reserve in eastern Kenya and Mikumi National Park, central Tanzania. The six loci (D1S158, D2S144, D4S243, D5S1466, D16S508, and D17S804) were all originally cloned from and characterized in the human genome. These microsatellites are polymorphic in both baboon populations, with the average heterozygosity across loci equal to 0.731 in the Tana River sample and 0.787 in the Mikumi sample. The genetic differentiation between the two populations is substantial. Kolmogornov–Smirnov tests indicate that five of the six loci are significantly different in allele frequencies in the two populations. The mean F _ST across loci is 0.069, and Shriver's measure of genetic distance, which was developed for microsatellite loci (Shriver et al., 1995), is 0.255. This genetic distance is larger than corresponding distances among human populations residing in different continents. We conclude that (a) the arrays of alleles present at these six microsatellite loci in two geographically separated populations of yellow baboons are quite similar, but (b) the two populations exhibit significant differences in allele frequencies. This study illustrates the potential value of human microsatellite loci for analyses of population genetic structure in baboons and suggests that this approach will be useful in studies of other Old World monkeys.     

Identification of a QTL for Adipocyte Volume and of Shared Genetic Effects with Aspartate Aminotransferase

Plasma levels of aspartate aminotransferase (AST), a liver enzyme, are elevated in patients with visceral obesity. This study examined whether adipocyte volume is under the influence of genetic factors and evaluated its genetic correlations with AST. Fasting plasma levels of 344 pedigreed baboons from the Southwest National Primate Research Center in San Antonio, TX, USA, were assayed for AST. Adipocyte volume was measured using biopsies of omental adipose tissue. Adipocyte volume, body weight, and plasma AST were heritable. Genetic correlations between the measured adiposity-related phenotypes and AST were significant. A quantitative trait locus (LOD score 3.2) for adipocyte volume was identified on the baboon homolog of human chromosome 6 near marker D6S1028. These results suggest that omental adipocyte volume is under genetic regulation and that shared genetic factors influence adiposity-associated traits and AST.