Analysis of the heterochromatin of <Emphasis Type="Italic">Cebus</Emphasis> (Primates,Platyrrhini) by micro-FISH and banding pattern comparisons

The karyotype of the neotropical primate genus Cebus (Platyrrhini: Cebidae), considered the most ancestral one, shows the greatest amount of heterochromatin described among Platyrrhini genera. Banding techniques and restriction enzyme digestion have previously revealed great variability of quantity and composition of heterochromatin in this genus. In this context, we use fluorescence in situ hybridization (FISH) to analyse this genomic region and discuss its possible role in the diversification of Cebus. We used a heterochromatin probe for chromosome 11 of Cebus libidinosus (11qHe+ CLI probe), obtained by chromosome microdissection. Twenty-six specimens belonging to the families Atelidae, Cebidae, Callitrichidae and Pithecidae (Platyrrhini) were studied. Fourteen out of 26 specimens were Cebus (Cebidae) individuals of C. libidinosus, C. xanthosternos, C. apella, C. nigritus, C. albifrons, C. kaapori and C. olivaceus. In Cebus specimens, we found 6 to 22 positive signals located in interstitial and telomeric positions along the different species. No hybridization signal was observed among the remaining Ceboidea species, thus reinforcing the idea of a Cebus-specific heterochromatin composed of a complex system of repetitive sequences.     

When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini)

Background

How are morphological evolution and developmental changes related? This rather old and intriguing question had a substantial boost after the 70s within the framework of heterochrony (changes in rates or timing of development) and nowadays has the potential to make another major leap forward through the combination of approaches: molecular biology, developmental experimentation, comparative systematic studies, geometric morphometrics and quantitative genetics. Here I take an integrated approach combining life-history comparative analyses, classical and geometric morphometrics applied to ontogenetic series to understand changes in size and shape which happen during the evolution of two New World Monkeys (NWM) sister genera.

Results

Cebus and Saimiri share the same basic allometric patterns in skull traits, a result robust to sexual and ontogenetic variation. If adults of both genera are compared in the same scale (discounting size differences) most differences are small and not statistically significant. These results are consistent using both approaches, classical and geometric Morphometrics. Cebus is a genus characterized by a number of peramorphic traits (adult-like) while Saimiri is a genus with paedomorphic (child like) traits. Yet, the whole clade Cebinae is characterized by a unique combination of very high pre-natal growth rates and relatively slow post-natal growth rates when compared to the rest of the NWM. Morphologically Cebinae can be considered paedomorphic in relation to the other NWM. Geometric morphometrics allows the precise separation of absolute size, shape variation associated with size (allometry), and shape variation non-associated with size. Interestingly, and despite the fact that they were extracted as independent factors (principal components), evolutionary allometry (those differences in allometric shape associated with intergeneric differences) and ontogenetic allometry (differences in allometric shape associated with ontogenetic variation within genus) are correlated within these two genera. Furthermore, morphological differences produced along these two axes are quite similar. Cebus and Saimiri are aligned along the same evolutionary allometry and have parallel ontogenetic allometry trajectories.

Conclusion

The evolution of these two Platyrrhini monkeys is basically due to a size differentiation (and consequently to shape changes associated with size). Many life-history changes are correlated or may be the causal agents in such evolution, such as delayed on-set of reproduction in Cebus and larger neonates in Saimiri.     

On the occurrence of Cebus flavius (Schreber 1774) in the Caatinga, and the use of semi-arid environments by Cebus species in the Brazilian state of Rio Grande do Norte

Cebus flavius is a recently rediscovered species and a candidate for the 25 most endangered primate species list. It was hypothesized that the distribution of C. flavius was limited to the Atlantic Forest, while the occurrence of C. libidinosus in the Rio Grande do Norte (RN) Caatinga was inferred, given its occurrence in neighboring states. As a result of a survey in ten areas of the RN Caatinga, this paper reports on four Cebus populations, including the first occurrence of C. flavius in the Caatinga, and an expansion of the northwestern limits of distribution for the species. This C. flavius population may be a rare example of a process of geographic distribution retraction, and is probably the most endangered population of this species. New areas of occurrence of C. libidinosus are also described. Tool use sites were observed in association with reports of the presence of both capuchin species.     

A comparative study of the recombination pattern in three species of Platyrrhini monkeys (primates)

Homologous chromosomes exchange genetic information through recombination during meiotic synapsis, a process that increases genetic diversity and is fundamental to sexual reproduction. Meiotic studies in mammalian species are scarce and mainly focused on human and mouse. Here, the meiotic recombination events were determined in three species of Platyrrhini monkeys (Cebus libidinosus, Cebus nigritus and Alouatta caraya) by analysing the distribution of MLH1 foci at the stage of pachytene. Moreover, the combination of immunofluorescence and fluorescent in situ hybridisation has enabled us to construct recombination maps of primate chromosomes that are homologous to human chromosomes 13 and 21. Our results show that (a) the overall number of MLH1 foci varies among all three species, (b) the presence of heterochromatin blocks does not have a major influence on the distribution of MLH1 foci and (c) the distribution of crossovers in the homologous chromosomes to human chromosomes 13 and 21 are conserved between species of the same genus (C. libidinosus and C. nigritus) but are significantly different between Cebus and Alouatta. This heterogeneity in recombination behaviour among Ceboidea species may reflect differences in genetic diversity and genome composition.     

Fallback foraging as a way of life: Using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly “specialized” taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods. Am J Phys Anthropol 140:687–699, 2009. © 2009 Wiley-Liss, Inc.     

Variation in Body Shape across Species and Populations in a Radiation of Diaptomid Copepods

Inter and intra-population variation in morphological traits, such as body size and shape, provides important insights into the ecological importance of individual natural populations. The radiation of Diaptomid species (~400 species) has apparently produced little morphological differentiation other than those in secondary sexual characteristics, suggesting sexual, rather than ecological, selection has driven speciation. This evolutionary history suggests that species, and conspecific populations, would be ecologically redundant but recent work found contrasting ecosystem effects among both species and populations. This study provides the first quantification of shape variation among species, populations, and/or sexes (beyond taxonomic illustrations and body size measurements) to gain insight into the ecological differentiation of Diaptomids. Here we quantify the shape of five Diaptomid species (family Diaptomidae) from four populations each, using morphometric landmarks on the prosome, urosome, and antennae. We partition morphological variation among species, populations, and sexes, and test for phenotype-by-environment correlations to reveal possible functional consequences of shape variation. We found that intraspecific variation was 18-35% as large as interspecific variation across all measured traits. Interspecific variation in body size and relative antennae length, the two traits showing significant sexual dimorphism, were correlated with lake size and geographic location suggesting some niche differentiation between species. Observed relationships between intraspecific morphological variation and the environment suggest that divergent selection in contrasting lakes might contribute to shape differences among local populations, but confirming this requires further analyses. Our results show that although Diaptomid species differ in their reproductive traits, they also differ in other morphological traits that might indicate ecological differences among species and populations.     

Genetic and morphological differentiation in the clam Coelomactra antiquata (Bivalvia: Veneroida) along the coast of China

Coelomactra antiquata is a commercially exploited bivalve, and its populations have been severely declining in the coast of China during the last two decades. In order to provide guidelines for conservation strategies and management programs, four populations of C. antiquata, representing the most important populations in China, were analysed morphologically and genetically to reveal the genetic structure by using 7 polymorphic allozyme loci and 12 morphological variables. The mean allele richness ranged from 2.79 to 3.53, while the mean heterozygosity ranged from 0.326 to 0.519. All genetic distance metrics revealed high level of genetic differentiation between the three northern populations and one southern population. The marked genetic differentiation can be explained by the freshwater outflow of Yangtze River and upwelling of Zhejiang province. The morphological analyses were in accordance with the allozyme data, which also disclosed a high degree of differentiation between the northern and southern populations. The results obtained in this study indicate that the northern and southern populations in C. antiquata should be treated as separate units for conservation management.     

Distance between south-European and south-west Asiatic refugial areas involved morphological differentiation: Pinus sylvestris case study

The phenotypic differentiation of relic P. sylvestris in southern Europe and southwestern Asia was verified using thirty-two populations sampled from the Iberian Peninsula, Massif Central, Balkan Peninsula, Crimea and Anatolia. Twenty-one morphological and anatomical needle traits and 18 cone morphological characteristics were examined to describe the population diversity and differentiation. The needle characters were not correlated to those of cone. The differences between regions were significant based on 12 needle and 9 cone characteristics, suggesting spatial isolation. The differentiation between the Iberian and Anatolian populations was the highest, which indicates the isolation by distance. The high level of morphological differentiation was also found among Iberian populations, supporting the already known complex history of the species in that region. Populations within other regions were differentiated at lower levels; however, the West Anatolian populations differed morphologically from the eastern ones. The described pattern of morphological differentiation supports the idea of the long-lasting existence of P. sylvestris in the south-European and Anatolian mountain regions. To conserve this variation, seed transfer between regions in the forest economy should be restricted.     

Does isolation affect phenotypic variability and fluctuating asymmetry in the endangered Red Apollo?

Isolated populations represent one of the main focuses in conservation biology. Long-term isolation often causes losses of genetic diversity and as a consequence might reduce individual fitness. Morphometric characters can be used as suitable markers to analyse ecological stress and individual fitness of local populations. Asymmetry in bilateral symmetry is used as a measure for developmental instability of populations and is often negatively correlated with population size and low genetic diversity. As a study system, we selected the endangered butterfly Parnassius apollo, which occurs in small and isolated remnant populations in Central Europe, but also in fairly large metapopulations in the Alps. We analysed wing morphometrics (shape and size characters) of 812 individuals representing (1) already extinct, (2) highly isolated and (3) still interconnected populations. Seventeen landmarks on veins were used to analyse morphological variances in the wing shape. Our data show significant deviations between landmarks on the left and right wing side within individuals and strong morphological variance among individuals. The highest morphological variability could be found for individuals in the Alps, however, the level of asymmetry was very similar for all populations analysed. The higher morphological variability found in the Alps can be interpreted as a consequence of the higher level of the genetic diversity detectable for this region. Analysis on morphological variance of P. apollo individuals of the Mosel valley using time series ranging from 1895 until today showed no significant rise in asymmetry and no decline of morphological variability over time, although, anthropogenic habitat destruction has caused severe bottlenecks in this population.     

The emissary foramina: Their value in platyrrhine systematics

A discriminant analysis was performed on 226 ceboid skulls using data on emissary foramina size and shape. The purposes of the study are to 1) measure the success with which these discriminating variables can distinguish among platyrrhine genera and 2) derive a set of classification functions which will permit the classification of new cases with unknown group membership (i.e., fossil skulls). This technique is able to correctly classify 80% of the 226 ceboid skulls. Support is given to the allocation of Chiropotes, Cacajao, and Pithecia into one morphologically unified subfamily, Pitheciinae. Alouatta, Ateles, and Lagothrix also share many similarities in emissary foramina size and shape and their inclusion into one subfamily, Atelinae, is probably warranted. The distinctiveness of Cebus in these same morphological features is apparent. Possibilities for extending this procedure to study fossil lineages in platyrrhines are discussed.     

Population genetic structure of sharpbelly Hemiculter leucisculus (Basilesky, 1855) and morphological diversification along climate gradients in China

Sharpbelly Hemiculter leucisculus (Basilewski, 1855) is a small, widespread, and native cyprinid fish with prominent habitat suitability and high invasive potential and is becoming the dominant species in freshwater ecosystems under intensified environmental disturbances. But how H. leucisculus acclimates to extremely heterogeneous environments remains unclear. In current study, the genetic structure of H. leucisculus was analyzed using Bayesian phylogenetic inference, haplotype network, and STRUCTURE base on cytb gene across 18 populations spanning 20 degrees of latitude and 18 degrees of longitude in China. The morphological diversification of body size and shape for H. leucisculus along the climate gradient was studied. The results showed that the 18 H. leucisculus populations were divided into 3 clusters: one cluster mainly from Huanghe River Basin, another cluster mainly from Yangzi River Basin, and H cluster containing Hainan and Beihai populations. The fish from southern populations were deeper bodied while individuals from northern populations were more slender. Inland individuals were more streamlined while coastal individuals were of deeper body. The partial Mantel test predicts that the potential mechanism underlining the intraspecies morphological diversification along climate gradients is primarily the divergent selection pressures among different environments, while genetic variation had less contribution to morphological differentiation. The formation of the Nanling Mountain Range could drive genetic differentiation between Beihai population and those from Yangzi River Basin. The present results highlight strong selective pressures of climate on widespread species and enrich morphological differentiation basis of acclimation for species with high habitat suitability and invasive potential.     

Morphological and Genetic Divergences in a Coral Reef Damselfish, Pomacentrus coelestis

Population differentiation is one of the main topics in evolutionary biology. Except the exploration of color variation, few studies focused on morphological divergences among populations of coral reef fishes. In this work, we studied morphological and genetic differentiation among populations of the damselfish, Pomacentrus coelestis, in the northwestern Pacific Ocean. The shapes of the mandible and the premaxilla were explored using geometric morphometric methods and the genetic structure was investigated using microsattelites. Various tests revealed significant shape variation among most P. coelestis populations for both skeletal units. Morphological variation of the mandible accompanies a genetic break between populations of mainland Japan and Okinawa-Taiwan. However, Mantel and Procrustes tests revealed no congruence between morphological and genetic structures. We illustrate that phenotypic plasticity and adaptive divergence are potential evolutionary mechanisms underlying shape difference among P. coelestis populations. An ecomorphological approach suggests that various diet could be related to shape variation of oral jaws.     

Cryptic structure and niche divergence within threatened Galápagos giant tortoises from southern Isabela Island

Although Galápagos giant tortoises are an icon for both human-mediated biodiversity losses and conservation management successes, populations of two species on southern Isabela Island (Chelonoidis guntheri, and C. vicina) remain threatened by hunting and persistence of feral animals. Conservation management of these tortoises has been hampered by lack of clarity regarding their taxonomy, ecological and morphological diversity, and the spatial distribution of evolutionarily significant units that may exist. Analyses of 16 microsatellite loci did not group samples according to current taxonomy. Instead, three (rather than two) genetic clusters were revealed. We show that the three regions of southern Isabela associated with these genetic clusters are significantly different in their ecological niches, which could suggest that ecological divergence may have shaped patterns of genetic differentiation in these tortoises. Furthermore, results suggest limited recent gene flow among sampled localities and between each of the three regions associated with genetic clusters. We discuss the need for further research on the ecological factors shaping the genetic and morphological diversity of southern Isabela tortoises. We suggest that current strategies whereby populations are managed separately are warranted pending further study, but due to mixed ancestry we recommend that Cerro Paloma tortoises be excluded from management programs.     

Wildlife uses and hunting patterns in rural communities of the Yucatan Peninsula, Mexico

Background

Use of plant resources and ecosystems practiced by indigenous peoples of Mesoamerica commonly involves domestication of plant populations and landscapes. Our study analyzed interactions of coexisting wild and managed populations of the pitaya Stenocereus pruinosus, a columnar cactus used for its edible fruit occurring in natural forests, silviculturally managed in milpa agroforestry systems, and agriculturally managed in homegardens of the Tehuacán Valley, Mexico. We aimed at analyzing criteria of artificial selection and their consequences on phenotypic diversity and differentiation, as well as documenting management of propagules at landscape level and their possible contribution to gene flow among populations.

Methods

Semi-structured interviews were conducted to 83 households of the region to document perception of variation, criteria of artificial selection, and patterns of moving propagules among wild and managed populations. Morphological variation of trees from nine wild, silviculturally and agriculturally managed populations was analyzed for 37 characters through univariate and multivariate statistical methods. In addition, indexes of morphological diversity (MD) per population and phenotypic differentiation (PD) among populations were calculated using character states and frequencies.

Results

People recognized 15 pitaya varieties based on their pulp color, fruit size, form, flavor, and thorniness. On average, in wild populations we recorded one variety per population, in silviculturally managed populations 1.58 ± 0.77 varieties per parcel, and in agriculturally managed populations 2.19 ± 1.12 varieties per homegarden. Farmers select in favor of sweet flavor (71% of households interviewed) and pulp color (46%) mainly red, orange and yellow. Artificial selection is practiced in homegardens and 65% of people interviewed also do it in agroforestry systems. People obtain fruit and branches from different population types and move propagules from one another. Multivariate analyses showed morphological differentiation of wild and agriculturally managed populations, mainly due to differences in reproductive characters; however, the phenotypic differentiation indexes were relatively low among all populations studied. Morphological diversity of S. pruinosus (average MD = 0.600) is higher than in other columnar cacti species previously analyzed.

Conclusions

Artificial selection in favor of high quality fruit promotes morphological variation and divergence because of the continual replacement of plant material propagated and introduction of propagules from other villages and regions. This process is counteracted by high gene flow influenced by natural factors (pollinators and seed dispersers) but also by human management (movement of propagules among populations), all of which determines relatively low phenotypic differentiation among populations. Conservation of genetic resources of S. pruinosus should be based on the traditional forms of germplasm management by local people.     

Population genetics of bisexual and unisexual populations of the scaly-winged bark louse Echmepteryx hageni (Insecta: Psocoptera)

The scaly-winged bark louse, Echmepteryx hageni, exhibits a unique pattern of co-existence of apparently differnt reproductive modes. Unisexuality is widespread in eastern North America, while sexual populations are restricted to isolated rock out-croppings in southern Illinois and eastern Kentucky. Three of the four nuclear loci examined show greater genetic diversity in the unisexual form compared to the sexual form of E. hageni, in accordance with the pattern previously shown in mitochondrial genetic data. Neutrality tests of the nuclear loci indicate a consistent signal of demographic expansion in asexual populations, but not in sexual populations. There was evidence of inbreeding in the isolated sexual populations at three of the nuclear loci, and one locus had signs of gene specific balancing selection. However, there is no significant genetic differentiation between bisexual and unisexual populations, possibly due to the greater effective population size of nuclear loci relative to mitochondrial loci. The mitochondrial differentiation of E. hageni populations in the northwestern part of their range (Minnesota and Wisconsin) was also not reflected in the nuclear data. We present three hypotheses that may explain the disparity in observed nuclear and mitochondrial genetic diversity between the reproductive forms of E. hageni.     

Symmetry and asymmetry in fingerprints of three genera of South American monkeys in relation to morphological evolutionary problems

Fingerprints of South American monkeys of the genera Alouatta, Ateles and Cebus were studied. Dermatoglyphics were analysed in relation to pattern intensities; the distribution of symmetric and asymmetric designs was also determined. Results have been related to some aspects of the contribution of dermatoglyphics to the study of Primate morphological evolution.     

Activity Patterns,Home Range Size,and Intergroup Encounters in <Emphasis Type="Italic">Cebus albifrons</Emphasis> Support Existing Models of Capuchin Socioecology

Variation in ranging behavior, social organization, and feeding ecology among capuchins (Cebus spp.) is a classic example of how closely related species may be differentially adapted to their local environments. Marked differences in all 3 areas occur among Cebus spp. between the untufted capuchins (Cebus capucinus, C. olivaceous, and C. albifrons) and the tufted capuchins (C. apella, C. xanthosternos, C. nigritus, and C. libidinosus). The key socioecological distinction between the 2 groups has traditionally been that, compared with the tufted group, untufted capuchins eat more ripe foods, as befits their more gracile masticatory system; range more broadly in search of high-quality foods; and live in larger groups with more males and more agonistic interactions between groups. Here I assess how well the basic socioecological characteristics —activity budget, ranging— of previously unstudied Ecuadorian Cebus albifrons fit within this model. Few researchers have conducted studies on Cebus albifrons, despite its prominent role in the initial development of the model for socioecology of Cebus. The results of my 1-yr study of a single social group support the model’s general characterization of untufted capuchins in ranging and feeding behaviors, but also suggest that direct ecological and demographic effects, in addition to adaptation to local conditions, may explain additional variation in group size across species of Cebus.     

Genetic structure of peripheral, island-like populations: a case study of Saponaria bellidifolia Sm. (Caryophyllaceae) from the Southeastern Carpathians

Geographically peripheral populations often experience a reduction of genetic diversity and divergence from the core populations. Habitat geometry and quality can induce a local genetic diversity pattern, which overlies the regional variability issued from the range-wide phylogeography. We evaluated the genetic variation and genetic divergence of Saponaria bellidifolia Sm. on limestone outcrops within peripheral island-like populations from the Southeastern Carpathians, using RAPD markers. We also determined the degree of isolation related to other European populations, using AFLP. The Romanian populations had a decreased overall genetic diversity shared among populations, with lower level in small populations. Potential habitat size had a positive effect on genetic diversity estimates. Fisher’s exact tests of genetic differentiation revealed significant divergences only between the geographically most distant populations. Romanian populations were genetically pauperised as compared to Bulgarian and Italian populations and our results suggest that they might have originated from a recent range expansion from southern glacial refugia.     

基于形态及分子标记的濒危植物夏蜡梅自然居群的遗传变异研究

比较了濒危植物夏蜡梅(Sinocalycanthus chinensis)大明山、大雷山、龙须山3个居群的果实与种子的形态变异,采用ISSR分子标记技术分析DNA序列的变异,综合评价夏蜡梅3个居群的遗传变异。结果如下:果实性状中,果柄长、果实长、果实重、每果种子数等指标均以大明山居群最大、大雷山居群次之、龙须山居群最小,它们之间差异显著(P<0.05)。种子重、种子长、种子宽、种子厚等指标均以大雷山居群最大,与大明山居群和龙须山居群差异显著(P<0.05)。基于果实形态特征的表型分化系数(VST)在0.5518—0.9750之间,平均为0.8930,所有果实形态指标的变异大部分存在于居群间。基于种子形态特征的VST在0.1669—0.8678之间,平均为0.6240,除种子长外,其他种子形态指标的变异也大部分存在于居群间。ISSR分析表明,3个居群的多态位点百分率、Shannon信息指数、Nei基因多样性均是大明山居群最高、龙须山居群次之、大雷山居群最低。居群间的遗传分化系数(GST)为0.6050。基于ISSR分子标记数据的聚类结果显示大明山居群先与龙须山居群聚在一起,再与大雷山居群相聚,这与基于种子性状特征的聚类结果相似,而与基于果实性状特征的聚类结果不同。3个居群的种子形态特征变异系数与遗传多样性水平具有显著的正相关,且基于果实形态特征估算的VST要高于GST,而基于种子形态特征估算的VST仅略高于GST,表明夏蜡梅不同居群间的种子形态变异主要由遗传变异所造成的,而环境因子在果实形态变异中起了重要作用。Mantel检验显示3个居群基于分子标记数据的遗传距离矩阵和基于果实及种子形态特征的欧氏距离矩阵之间的相关性不显著,表明果实与种子在居群间出现的表型分化除了受遗传因素影响外,还受到其它环境因子的强烈影响。