Disparate and parallel craniofacial climatic adaptations in native populations of Asia, North America, and South America.

Understanding the impact that climate had in shaping cranial variation is critical for inferring the evolutionary mechanisms that played a role in human diversification. Here, we provide a comprehensive study aiming to analyze the association between climate and cranial variation of high latitude populations living in temperate to cold environments of Asia, North America, and South America. For this, we compiled a large morphometric dataset (N = 2633), which was combined with climatic and genomic data. We tested the influence of climate on the facial skeleton, nasal protrusion, and cranial vault and through multiple statistical tests at two geographical scales: intracontinental and intercontinental. We show that populations living in cold areas share a morphological pattern characterized by an increase in nasal height, facial and orbital heights and widths, a decrease in facial protrusion, and larger, longer, and lower cranial vaults. There are also distinctive features; populations from north Asia present the tallest noses, largest faces, and cranial vaults of the whole sample. Nasal breadth dimensions show small values in Asians, large values in South Americans, and non-significant changes in arctic North America. The morphological pattern in populations living at high latitude may be the result of parallel adaptation, as supported by physiological, morphometric, ecological, and genetic explanations, while the differences in magnitude and phenotypic expression could be due to the diverse population histories, severity of climate, and cultural strategies. Overall, our study shows that climate is a relevant factor shaping modern human morphology and it should be considered when studying modern human evolution and diversification.

Evolution, divergence, and convergence in the mandibles of opossums (Didelphidae, Didelphimorphia).

Didelphid marsupials are considered a morphologically unspecialized group with a generalist diet that includes vertebrates, invertebrates, and plant matter. While cranium and scapula variation has already been examined within Didelphidae, variation in mandible shape, usually associated with diet or phylogeny in other mammalian groups, has not yet been properly assessed in the family. We evaluated the variation in mandible shape and size of didelphids (2470 specimens belonging to 94 species) using 2D geometric morphometrics. We classified the diet of the didelphids into four broad categories to assess whether morphospace ordination relates to dietary habits. We also provided the most comprehensive phylogeny for the family (123 out of the 126 living species) using 10 nuclear and mitochondrial genes. We then mapped mandible size and shape onto that phylogeny for 93 selected taxa and ancestral size and shapes were reconstructed by parsimony. We found phylogenetically structured variation in mandible morphology between didelphid groups, and our results indicate that they have a significant phylogenetic signal. The main axis of shape variation is poorly related to size, but the second is strongly allometric, indicating that allometry is not the main factor in shaping morphological diversity on their mandibles. Our results indicate that the shape and size of the ancestral mandible of didelphids would be similar to that of the current species of the genus Marmosa.

Replicated radiations in the South American marsh pitcher plants (Heliamphora) lead to convergent carnivorous trap morphologies.

PREMISE: The evolution of carnivorous pitcher traps across multiple angiosperm lineages represents a classic example of morphological convergence. Nevertheless, no comparative study to-date has examined pitcher evolution from a quantitative morphometric perspective. METHODS: In the present study, we used comparative morphometric approaches to quantify the shape space occupied by Heliamphora pitchers and to trace evolutionary trajectories through this space to examine patterns of divergence and convergence within the genus. We also investigated pitcher development, and, how the packing of pitchers is affected by crowding, a common condition in their natural environments. RESULTS: Our results showed that Heliamphora pitchers have diverged along three main axes in morphospace: (1) pitcher curvature; (2) nectar spoon elaboration; and (3) pitcher stoutness. Both curvature and stoutness are correlated with pitcher size, suggesting structural constraints in pitcher morphological evolution. Among the four traits (curvature, spoon elaboration, stoutness, and size), all but curvature lacked phylogenetic signal and showed marked convergence across the phylogeny. We also observed tighter packing of pitchers in crowded conditions, and this effect was most pronounced in curved, slender pitchers. CONCLUSIONS: Overall, our study demonstrates that diversification and convergent evolution of carnivory-related traits extends to finer evolutionary timescales, reinforcing the notion that ecological specialization may not necessarily be an evolutionary dead end.

The hidden links between animal weapons, fighting style, and their effect on contest success: a meta-analysis.

In many species that fight over resources, individuals use specialized structures to gain a mechanical advantage over their rivals during contests (i.e. weapons). Although weapons are widespread across animals, how they affect the probability of winning contests is still debated. According to theory, understanding weapon function during contests is essential to: (i) understanding its importance in determining the winner, and (ii) identifying what weapon traits (e.g. weapon length versus shape versus performance) are most relevant for contest success. However, quantitative evaluations of how weapon function affects the extent to which weapon traits influence contest success are still lacking. Here, we first develop an individual-based model to evaluate how increasing the influence of the weapon in determining the winner translates to differences between winners and losers. Then, we use a meta-analysis to identify: (i) whether different weapon measures influence contest outcome differently; (ii) how animals use their weapons during fights - i.e. weapon function; and (iii) if weapon function correlates to how weapons influence contest outcome. Our model showed that, as weapons increased the chance of determining the winner, the mean difference between winners and losers also increased. Therefore, in our meta-analysis we used the mean trait difference between winners and losers as a proxy for the extent to which weapons influence contest success. The literature search identified 49 suitable studies, containing information for 52 species, totalling 107 effect sizes. Four main patterns emerged. First, most of the literature focuses on linear measures of weapons, while performance measures are concentrated on Crustacea and Squamata; other types of measures were rare. Second, differences between winners and losers in linear measurements were greater than differences in performance measurements when all species were combined (and when we used only a subset). Third, species that bear weapons almost always perform visual/tactile displays before engaging in physical contact. And fourth, while the way individuals display their weapons did not influence the importance of weapon size on contest outcomes, fighting style predicted when differences between winners and losers would be higher. Species that used their weapons to push or lift (even when combined with other functions) showed greater differences between winners and losers when compared to species that used their weapons to impact, pierce, pull or squeeze. Overall, our results show that we have an incomplete understanding of animal weapons built mostly on weapon size and a few select taxa. Thus, we should start focusing on measuring weapons according to how they are used during contests and in a wider diversity of species. One way forward is to conduct studies that integrate weapon morphology to weapon function to ensure we are measuring the most ecologically relevant variables.

Cis-regulatory variation in the shavenbaby gene underlies intraspecific phenotypic variation, mirroring interspecific divergence in the same trait.

Despite considerable progress in recent decades in dissecting the genetic causes of natural morphological variation, there is limited understanding of how variation within species ultimately contributes to species differences. We have studied patterning of the non-sensory hairs, commonly known as "trichomes," on the dorsal cuticle of first-instar larvae of Drosophila. Most Drosophila species produce a dense lawn of dorsal trichomes, but a subset of these trichomes were lost in D. sechellia and D. ezoana due entirely to regulatory evolution of the shavenbaby (svb) gene. Here, we describe intraspecific variation in dorsal trichome patterns of first-instar larvae of D. virilis that is similar to the trichome pattern variation identified previously between species. We found that a single large effect QTL, which includes svb, explains most of the trichome number difference between two D. virilis strains and that svb expression correlates with the trichome difference between strains. This QTL does not explain the entire difference between strains, implying that additional loci contribute to variation in trichome numbers. Thus, the genetic architecture of intraspecific variation exhibits similarities and differences with interspecific variation that may reflect differences in long-term and short-term evolutionary processes.

Phylogenomics in Cactaceae: A case study using the chollas sensu lato (Cylindropuntieae, Opuntioideae) reveals a common pattern out of the Chihuahuan and Sonoran deserts.

PREMISE: Although numerous phylogenetic studies have been conducted in Cactaceae, whole-plastome datasets have not been employed. We used the chollas to develop a plastome dataset for phylogeny reconstruction to test species relationships, biogeography, clade age, and morphological evolution. METHODS: We developed a plastome dataset for most known diploid members of the chollas (42 taxa) as well as for other members of Cylindropuntieae. Paired-end, raw reads from genome skimming were reference-mapped onto a de novo plastome assembly of one species of cholla, Cylindropuntia bigelovii, and were used to build our plastome dataset, which was analyzed using various methods. RESULTS: Our plastome dataset resolved the phylogeny of the chollas, including most interspecific and intraspecific relationships. Tribe Cylindropuntieae arose ~18 mya, during the early Miocene in southern South America, and is supported as sister to the South American clade Tephrocacteae. The (Micropuntia (Cylindropuntia + Grusonia)) clade most likely originated in the Chihuahuan Desert region around 16 mya and then migrated into other North American desert regions. Key morphological characters for recognizing traditional taxonomic series in Cylindropuntia (e.g., spiny fruit) are mostly homoplasious. CONCLUSIONS: This study provides the first comprehensive plastome phylogeny for any clade within Cactaceae. Although the chollas s.l. are widespread throughout western North American deserts, their most recent common ancestor likely arose in the Chihuahuan Desert region during the mid-Miocene, with much of their species diversity arising in the early to mid-Pliocene, a pattern strikingly similar to those found in other western North American desert groups.

Ancient and contingent body shape diversification in a hyperdiverse continental fish radiation.

The characiform fishes of the Neotropics and Africa radiated remarkably in ecomorphology, but the macroevolutionary processes responsible for their biodiversity remain unexplored, and the degree to which their continental diversification parallels classic adaptive radiations remains untested. We reconstruct their diversification using a new fossil-calibrated molecular phylogeny, dietary information, and geometric morphometrics. Though body shape diversified early in a manner consistent with an ancient continental adaptive radiation, trophic shifts did not always coincide with shape changes. With the notable exception of piscivores, lineages that converged in diet did not converge closely in body shape. Shifts in habitat or other variables likely influenced body shape evolution in addition to changes in diet, and the clade's history departs from many classic adaptive radiations in lakes or on islands, in which trophic convergence drives morphological convergence. The contrast between the Neotropical radiation's exhaustive exploration of morphospace and the more restrained diversification in Africa suggests a major role for contingency in characiform evolution, with the presence of cypriniform competitors in the Old World, but not the New, providing one possible explanation. Our results depict the clearest ecomorphological reconstruction to date for Characiformes and set the stage for studies further elucidating the processes underlying its diversification.

The Laterosensory Canal System in Epigean and Subterranean Ituglanis (Siluriformes: Trichomycteridae), With Comments About Troglomorphism and the Phylogeny of the Genus.

The laterosensory system is a mechanosensory modality involved in many aspects of fish biology and behavior. Laterosensory perception may be crucial for individual survival, especially in habitats where other sensory modalities are generally useless, such as the permanently aphotic subterranean environment. In the present study, we describe the laterosensory canal system of epigean and subterranean species of the genus Ituglanis (Siluriformes: Trichomycteridae). With seven independent colonizations of the subterranean environment in a limited geographical range coupled with a high diversity of epigean forms, the genus is an excellent model for the study of morphological specialization to hypogean life. The comparison between epigean and subterranean species reveals a trend toward reduction of the laterosensory canal system in the subterranean species, coupled with higher intraspecific variability and asymmetry. This trend is mirrored in other subterranean fishes and in species living in different confined spaces, like the interstitial environment. Therefore, we propose that the reduction of the laterosensory canal system should be regarded as a troglomorphic (= cave-related) character for subterranean fishes. We also comment about the patterns of the laterosensory canal system in trichomycterids and use the diversity of this system among species of Ituglanis to infer phylogenetic relationships within the genus. J. Morphol. 278:4-28, 2017. ©© 2016 Wiley Periodicals,Inc.

Morphological Integration of the Orbital Region in a Human Ontogenetic Sample.

Most studies on craniofacial morphology have focused on adult individuals, but patterns of variation are the outcome of genetic and epigenetic variables that interact throughout ontogeny. Among cranial regions, the orbits exhibit morphological variation and occupy an intermediate position between neurocranial and facial structures. The main objective of this work was to analyze postnatal ontogenetic variation and covariation in the morphology of the orbital region in a cross-sectional series of humans from 0 to 31 years old. Landmarks and semilandmarks were digitized on the orbital rim, as well as in neighboring neural and facial structures. Data were analyzed using geometric morphometrics. Results indicated that orbital size increases during the first years of postnatal life, while the shape of the orbital aperture does not change significantly with age. In general, the pattern and magnitude of shape covariation do not vary markedly during postnatal life although some subtle shifts were documented. Additionally, the shape of the orbital aperture is more related to the anterior neurocranium than to zygomatic structures, even when the allometry is adjusted. Although we expected some influence from postnatal craniofacial growth and from some functional factors, such as mastication, on the development of the orbits, this assumption was not completely supported by our results. As a whole, our findings are in line with the prediction of an early influence of the eyes and extraocular tissues on orbital morphology, and could be interpreted in relation to processes promoting early neural development that coordinately affects orbital traits and the neurocranial skeleton.

EvolQG - An R package for evolutionary quantitative genetics.

We present an open source package for performing evolutionary quantitative genetics analyses in the R environment for statistical computing. Evolutionary theory shows that evolution depends critically on the available variation in a given population. When dealing with many quantitative traits this variation is expressed in the form of a covariance matrix, particularly the additive genetic covariance matrix or sometimes the phenotypic matrix, when the genetic matrix is unavailable and there is evidence the phenotypic matrix is sufficiently similar to the genetic matrix. Given this mathematical representation of available variation, the \textbf{EvolQG} package provides functions for calculation of relevant evolutionary statistics; estimation of sampling error; corrections for this error; matrix comparison via correlations, distances and matrix decomposition; analysis of modularity patterns; and functions for testing evolutionary hypotheses on taxa diversification.

Trichome structure and evolution in Neotropical lianas.

BACKGROUND AND AIMS: Trichomes are epidermal outgrowths generally associated with protection against herbivores and/or desiccation that are widely distributed from ferns to angiosperms. Patterns of topological variation and morphological evolution of trichomes are still scarce in the literature, preventing valid comparisons across taxa. This study integrates detailed morphoanatomical data and the evolutionary history of the tribe Bignonieae (Bignoniaceae) in order to gain a better understanding of current diversity and evolution of trichome types. METHODS: Two sampling schemes were used to characterize trichome types: (1) macromorphological characterization of all 105 species currently included in Bignonieae; and (2) micromorphological characterization of 16 selected species. Individual trichome morphotypes were coded as binary in each vegetative plant part, and trichome density and size were coded as multistate. Ancestral character state reconstructions were conducted using maximum likelihood (ML) assumptions. KEY RESULTS: Two main functional trichome categories were found: non-glandular and glandular. In glandular trichomes, three morphotypes were recognized: peltate (Pg), stipitate (Sg) and patelliform/cupular (P/Cg) trichomes. Non-glandular trichomes were uniseriate, uni- or multicellular and simple or branched. Pg and P/Cg trichomes were multicellular and non-vascularized with three clearly distinct cell layers. Sg trichomes were multicellular, uniseriate and long-stalked. ML ancestral character state reconstructions suggested that the most recent common ancestor (MRCA) of Bignonieae probably had non-glandular, Pg and P/Cg trichomes, with each trichome type presenting alternative histories of appearance on the different plant parts. For example, the MRCA of Bignonieae probably had non-glandular trichomes on the stems, prophylls, petiole, petiolule and leaflet veins while P/Cg trichomes were restricted to leaflet blades. Sg trichomes were not present in the MRCA of Bignonieae independently of the position of these trichomes. These trichomes had at least eight independent origins in tribe. CONCLUSIONS: The patterns of trichome evolution indicate that most morphotypes are probably homologous in Bignonieae and could be treated under the same name based on its morphological similarity and common evolutionary history, in spite of the plethora of names that have been previously designated in the literature. The trichome descriptions presented here will facilitate comparisons across taxa, allowing inferences on the relationsthips between trichome variants and future studies about their functional properties.

Phenotypic integration in flowers of neotropical lianas: diversification of form with stasis of underlying patterns.

Phenotypic integration is essential to the understanding of organismal evolution as a whole. In this study, a phylogenetic framework is used to assess phenotypic integration among the floral parts of a group of Neotropical lianas. Flowers consist of plant reproductive organs (carpels and stamens), usually surrounded by attractive whorls (petals and sepals). Thus, flower parts might be involved in different functions and developmental constraints, leading to conflicting selective forces. We found that Bignonieae flowers have very similar patterns of variance/covariance among traits and that such patterns are uncorrelated with the phylogenetic relationships between species. However, in spite of pattern stasis, our results also indicate that diversification of floral morphology in this group has occurred throughout the evolution of magnitudes of correlation among traits. Thus, we suggest that stabilizing selection has played an important role in phenotypic integration, resulting in the long-term stasis of covariance patterns underlying flower diversification during the ca. 50 Myr of evolution of Bignonieae. This is the first report of long-term stasis in the phenotypic integration of angiosperms, suggesting that patterns of floral morphology can be recognizable as specific attributes of distinct botanical families.