Sérgio F. dos Reis

Asymmetries in specialization in ant-plant mutualistic networks

Mutualistic networks involving plants and their pollinators or frugivores have been shown recently to exhibit a particular asymmetrical organization of interactions among species called nestedness: a core of reciprocal generalists accompanied by specialist species that interact almost exclusively with generalists. This structure contrasts with compartmentalized assemblage structures that have been verified in antagonistic food webs. Here we evaluated whether nestedness is a property of another type of mutualism—the interactions between ants and extrafloral nectary-bearing plants—and whether species richness may lead to differences in degree of nestedness among biological communities. We investigated network structure in four communities in Mexico. Nested patterns in ant–plant networks were very similar to those previously reported for pollination and frugivore systems, indicating that this form of asymmetry in specialization is a common feature of mutualisms between free-living species, but not always present in species-poor systems. Other ecological factors also appeared to contribute to the nested asymmetry in specialization, because some assemblages showed more extreme asymmetry than others even when species richness was held constant. Our results support a promising approach for the development of multispecies coevolutionary theory, leading to the idea that specialization may coevolve in different but simple ways in antagonistic and mutualistic assemblages.

Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks

The structure of mutualistic networks provides clues to processes shaping biodiversity [1-10]. Among them, interaction intimacy, the degree of biological association between partners, leads to differences in specialization patterns [4, 11] and might affect network organization [12]. Here, we investigated potential consequences of interaction intimacy for the structure and coevolution of mutualistic networks. From observed processes of selection on mutualistic interactions, it is expected that symbiotic interactions (high-interaction intimacy) will form species-poor networks characterized by compartmentalization [12, 13], whereas nonsymbiotic interactions (low intimacy) will lead to species-rich, nested networks in which there is a core of generalists and specialists often interact with generalists [3, 5, 7, 12, 14]. We demonstrated an association between interaction intimacy and structure in 19 ant-plant mutualistic networks. Through numerical simulations, we found that network structure of different forms of mutualism affects evolutionary change in distinct ways. Change in one species affects primarily one mutualistic partner in symbiotic interactions but might affect multiple partners in nonsymbiotic interactions. We hypothesize that coevolution in symbiotic interactions is characterized by frequent reciprocal changes between few partners, but coevolution in nonsymbiotic networks might show rare bursts of changes in which many species respond to evolutionary changes in a single species.

NETWORK ANALYSIS REVEALS CONTRASTING EFFECTS OF INTRASPECIFIC COMPETITION ON INDIVIDUAL VS. POPULATION DIETS

Optimal foraging theory predicts that individuals should become more opportunistic when intraspecific competition is high and preferred resources are scarce. This density-dependent diet shift should result in increased diet breadth for individuals as they add previously unused prey to their repertoire. As a result, the niche breadth of the population as a whole should increase. In a recent study, R. Svanbäck and D. I. Bolnick confirmed that intraspecific competition led to increased population diet breadth in threespine stickleback (Gasterosteus aculeatus). However, individual diet breadth did not expand as resource levels declined. Here, we present a new method based on complex network theory that moves beyond a simple measure of diet breadth, and we use the method to reexamine the stickleback experiment. This method reveals that the population as a whole added new types of prey as stickleback density was increased. However, whereas foraging theory predicts that niche expansion is achieved by individuals accepting new prey in addition to previously preferred prey, we found that a subset of individuals ceased to use their previously preferred prey, even though other members of their population continued to specialize on the original prey types. As a result, populations were subdivided into groups of ecologically similar individuals, with diet variation among groups reflecting phenotype-dependent changes in foraging behavior as prey density declined. These results are consistent with foraging theory if we assume that quantitative trait variation among consumers affects prey preferences, and if cognitive constraints prevent individuals from continuing to use their formerly preferred prey while adding new prey.

Using δ13C stable isotopes to quantify individual-level diet variation

Individual-level diet variation can be easily quantified by gut-content analysis. However, because gut contents are a ‘snapshot’ of individuals’ feeding habits, such cross-sectional data can be subject to sampling error and lead one to overestimate levels of diet variation. In contrast, stable isotopes reflect an individual’s long-term diet, so isotope variation among individuals can be interpreted as diet variation. Nevertheless, population isotope variances alone cannot be directly compared among populations, because they depend on both the level of diet variation and the variance of prey isotope ratios. We developed a method to convert population isotope variances into a standardized index of individual specialization (WIC/TNW) that can be compared among populations, or to gut-content variation. We applied this method to diet and carbon isotope data of four species of frogs of the Brazilian savannah. Isotopes showed that gut contents provided a reliable measure of diet variation in three populations, but greatly overestimated diet variation in another population. Our method is sensitive to incomplete sampling of the prey and to among-individual variance in fractionation. Therefore, thorough sampling of prey and estimates of fractionation variance are desirable. Otherwise, the method is straightforward and provides a new tool for quantifying individual-level diet variation in natural populations that combines both gut-content and isotope data.

Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae)

Summary The rodent mandible has become a paradigm for studies on the development and evolution of complex morphological structures. We use a combination of geometric and multivariate morphometric methods in order to assess the correspondence between integration patterns and a priori biological models in the context of evolutionary shape divergence in the mandible of rodents of the family Echimyidae. The correlation of shape distances among operational taxonomic units (individuals, species, genera) in separate morphogenetic components allowed the construction of integration matrices among mandible components for data sets corresponding to varying levels of genetic divergence (intergeneric, interspecific, and intrapopulational). The integration matrices were associated with a priori biological (developmental, genetical, modular) models, and the maximum integration axes (singular warps) were compared with realized axes of maximum interspecific variation (relative warps). The integration pattern and intensity were not stable in data sets with different levels of genetic divergence, and the varying functional demands during the ecological radiation in the family were probably responsible for the differences in observed integration patterns. Developmental and genetic models were significantly associated with the interspecific integration patterns observed, suggesting a role for neutral evolution during the evolutionary divergence of mandible shape. However, directional and stabilizing selection were not discarded as processes responsible for the generation of interspecific integration. The choreography of the morphogenetic components in the mandible is highly flexible and the integrated groups of components can be reorganized depending on functional demands during evolutionary shape changes.

SKULL SHAPE AND SIZE DIVERGENCE IN DOLPHINS OF THE GENUS SOTALIA: A TRIDIMENSIONAL MORPHOMETRIC ANALYSIS

Abstract A study of cranial shape in dolphins of genus Sotalia was done using 104 specimens (92 from localities along the Brazilian coast and 12 from the Amazon River basin). Twenty-two cranial landmarks, assumed to be homologous, were selected for analysis. The first 2 principal components of aligned coordinates explained 40.6% of the total variation in cranial shape. Although no sexual dimorphism was detected (P = 0.811), shape differences among populations of Sotalia were highly significant (P < 0.000001). The 1st and 2nd principal components of shape showed that the Sotalia population from the Amazon basin differed in cranial shape from marine populations. Based on differences in geometric shape, a discriminant analysis of 3 linear measurements between landmarks provided an equation that classified skulls as belonging to Amazonian or marine populations. Based on these results and evidence from several other divergent character systems and life history attributes, we suggest the use of Sotalia guianensis for marine dolphins and S. fluviatilis for Amazonian dolphins.

Relationships among didelphid marsupials based on sequence variation in the mitochondrial cytochrome B gene

Variation in the mitochondrial cytochrome b gene (nucleotide and amino acid sequences) is evaluated for 9 genera and 15 species of American opossums in the family Didelphidae, using the American caenolestid rat opossumLestoros and the New Guinean peroryctid bandicootEchimypera as outgroups. Phylogenetic analyses (parsimony and distance) strongly support the monophyly of the Didelphidae and delineate two major clades; (1)Didelphis andPhilander are strongly aligned sister taxa, withMetachirus weakly but consistently associated with them, and (2)Marmosa plusMicoureus, withMonodelphis falling outside that pair. The generaMarmosops, Caluromys, andGlironia exhibit varied relationships, depending upon the method of analysis and data (DNA or amino acid sequences) used, but generally are placed individually or in combinations near or at the base of the didelphid radiation. Some aspects of these relationships are consistent with current taxonomic views, but others are in marked contrast. Specifically, a clade comprised of the mouse opossumsMarmosa, Micoureus, andMarmosops is strongly rejected by log-likelihood analysis, contrary to expectations from some current classifications. Also, the woolly opossumsCaluromys andGlironia also do not form a sister-taxon relationship, as suggested by their placement in a subfamily separate from the remaining didelphids examined. However, such a relationship cannot be rejected from log-likelihood analyses. The relationships suggested fromcyt-b sequences are strongly concordant with those based on DNA-DNA hybridization analyses. In addition to systematic and phylogenetic properties, molecular evolution of the didelphid cytochrome b gene sequence is characterized according to nucleotide bias and rate differentials at each codon position and across the entire sequence.

GEOMETRIC ESTIMATES OF HERITABILITY IN BIOLOGICAL SHAPE

Abstract The recently developed geometric morphometrics methods represent an important contribution of statistics and geometry to the study of biological shapes. We propose simple protocols using shape distances that incorporate geometric techniques into linear quantitative genetic models that should provide insights into the contribution of genetics to shape variation in organisms. The geometric approaches use Procrustes distances in a curved shape space and distances in tangent spaces within and among families to estimate shape heritability. We illustrate the protocols with an example of wing shape variation in the honeybee, Apis mellifera. The heritability of overall shape variation was small, but some localized components depicting shape changes on distal wing regions showed medium to large heritabilities. The genetic variance-covariance matrix of the geometric shape variables was significantly correlated with the phenotypic shape variance-covariance matrix. A comparison of the results of geometric methods with the traditional multivariate analysis of interlandmark distances indicated that even with a larger dimensionality, the interlandmark distances were not as rich in shape information as the landmark coordinates. Quantitative genetics studies of shape should greatly benefit from the application of geometric methods. Corresponding Editor: M. Zelditch

The nested structure of marine cleaning symbiosis: is it like flowers and bees?

In a given area, plant–animal mutualistic interactions form complex networks that often display nestedness, a particular type of asymmetry in interactions. Simple ecological and evolutionary factors have been hypothesized to lead to nested networks. Therefore, nestedness is expected to occur in other types of mutualisms as well. We tested the above prediction with the network structure of interactions in cleaning symbiosis at three reef assemblages. In this type of interaction, shrimps and fishes forage on ectoparasites and injured tissues from the body surface of fish species. Cleaning networks show strong patterns of nestedness. In fact, after controlling for species richness, cleaning networks are even more nested than plant–animal mutualisms. Our results support the notion that mutualisms evolve to a predictable community-level structure, be it in terrestrial or marine communities.

Environmental correlates of geographical variation in skull and mandible shape of the punaré rat Thrichomys apereoides (Rodentia: Echimyidae)

The pattern of correlations between geographic–environmental variables and geometric shape descriptors for the skull and mandible of Thrichomys apereoides was studied by recently developed combinations of geometry and multivariate statistical techniques. Environmental variables were obtained for each locality: altitude, mean temperature, rainfall, human population density, and vegetation type. The three views of the skull (dorsal, lateral and ventral) and the mandible were significantly associated with a latitudinal environmental gradient along the diagonal of open areas (caatinga and cerrado) throughout the range sampled. The populations from xeric environments presented relatively larger coronoid processes, larger jugals and wider snouts (related to the activity of jaw closing muscles). A correlation of patterns of shape variation from data sets of different skull views showed that lateral skull shape is the most informative view. Further studies are necessary to separate completely the contribution of genetic and environmental components to skull and mandible shape divergence among populations of T. apereoides.