Darter fishes exhibit variable intraspecific head shape allometry and modularity.

Allometry, the relationship between anatomical proportions and body size, may either limit or facilitate the diversification of morphology. We examined the impact of allometry in darter fish morphology, which displays a variety of trophic morphologies. This study aimed to address (a) whether there was significant variation in darter head allometry, (b) if allometry contributed to head shape diversity in adults, and (c) if darters show head shape modularity associated with allometry. We used geometric morphometrics to quantify head shape across 10 different species and test for heterogeneity in allometric slopes. In addition, we quantified the degree of modularity between the preorbital and postorbital regions of the darter head, both before and after correction for body size. We found that different species have unique allometric slopes, particularly among the Simoperca subgenus, and that closely related darter species tend to show ontogenetic divergence, contributing to the diversity of head shapes observed in adults. We suggest that such a pattern may result from the similarity of juvenile diets due to gape limitation. We also found that several species show significant modularity in head shape but that modularity was evolutionarily labile and only sometimes impacted by head shape allometry. Overall, our work suggests that ontogenetic shape development may have been important to the evolution of head shape in darters, particularly in the evolution of foraging traits and microhabitat.

Fruit odorants mediate co-specialization in a multispecies plant-animal mutualism.

Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats (Carollia spp.) and plants (Piper spp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models in Piper. Through behavioural assays, we found Carollia prefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of two Piper species highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropical Piper fruits evolved in tandem with seed dispersal by scent-oriented Carollia bats. Specifically, fruit scent chemistry in some Piper species fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent in Piper, our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity.

Mind the gap: natural cleft palates reduce biting performance in bats.

Novel morphological traits pose interesting evolutionary paradoxes when they become widespread in a lineage while being deleterious in others. Cleft palate is a rare congenital condition in mammals in which the incisor-bearing premaxilla bones of the upper jaw develop abnormally. However, ∼50% of bat species have natural, non-pathological cleft palates. We used the family Vespertilionidae as a model and linear and geometric morphometrics within a phylogenetic framework to (1) explore evolutionary patterns in cleft morphology, and (2) test whether cleft morphological variation is correlated with skull shape in bats. We also used finite element (FE) analyses to experimentally test how presence of a cleft palate impacts skull performance during biting in a species with extreme cleft morphology (hoary bat, Lasiurus cinereus). We constructed and compared the performance of two FE models: one based on the hoary bat's natural skull morphology, and another with a digitally filled cleft simulating a complete premaxilla. Results showed that cleft length and width are correlated with skull shape in Vespertilionidae, with narrower, shallower clefts seen in more gracile skulls and broader, deeper clefts in more robust skulls. FE analysis showed that the model with a natural cleft produced lower bite forces, and had higher stress and strain than the model with a filled cleft. In the rostrum, safety factors were 1.59-2.20 times higher in the model with a filled cleft than in the natural model. Our results demonstrate that cleft palates in bats reduce biting performance, and evolution of skull robusticity may compensate for this reduction in performance.

Anatomical diversification of a skeletal novelty in bat feet.

Neomorphic, membrane-associated skeletal rods are found in disparate vertebrate lineages, but their evolution is poorly understood. Here we show that one of these elements-the calcar of bats (Chiroptera)-is a skeletal novelty that has anatomically diversified. Comparisons of evolutionary models of calcar length and corresponding disparity-through-time analyses indicate that the calcar diversified early in the evolutionary history of Chiroptera, as bats phylogenetically diversified after evolving the capacity for flight. This interspecific variation in calcar length and its relative proportion to tibia and forearm length is of functional relevance to flight-related behaviors. We also find that the calcar varies in its tissue composition among bats, which might affect its response to mechanical loading. We confirm the presence of a synovial joint at the articulation between the calcar and the calcaneus in some species, which suggests the calcar has a kinematic functional role. Collectively, this functionally relevant variation suggests that adaptive advantages provided by the calcar led to its anatomical diversification. Our results demonstrate that novel skeletal additions can become integrated into vertebrate body plans and subsequently evolve into a variety of forms, potentially impacting clade diversification by expanding the available morphological space into which organisms can evolve.

3D Digitization in Functional Morphology: Where is the Point of Diminishing Returns?

Modern computational and imaging methods are revolutionizing the fields of comparative morphology, biomechanics, and ecomorphology. In particular, imaging tools such as X-ray micro computed tomography (µCT) and diffusible iodine-based contrast enhanced CT allow observing and measuring small and/or otherwise inaccessible anatomical structures, and creating highly accurate three-dimensional (3D) renditions that can be used in biomechanical modeling and tests of functional or evolutionary hypotheses. But, do the larger datasets generated through 3D digitization always confer greater power to uncover functional or evolutionary patterns, when compared with more traditional methodologies? And, if so, why? Here, we contrast the advantages and challenges of using data generated via (3D) CT methods versus more traditional (2D) approaches in the study of skull macroevolution and feeding functional morphology in bats. First, we test for the effect of dimensionality and landmark number on inferences of adaptive shifts during cranial evolution by contrasting results from 3D versus 2D geometric morphometric datasets of bat crania. We find sharp differences between results generated from the 3D versus some of the 2D datasets (xy, yz, ventral, and frontal), which appear to be primarily driven by the loss of critical dimensions of morphological variation rather than number of landmarks. Second, we examine differences in accuracy and precision among 2D and 3D predictive models of bite force by comparing three skull lever models that differ in the sources of skull and muscle anatomical data. We find that a 3D model that relies on skull µCT scans and muscle data partly derived from diceCT is slightly more accurate than models based on skull photographs or skull µCT and muscle data fully derived from dissections. However, the benefit of using the diceCT-informed model is modest given the effort it currently takes to virtually dissect muscles from CT scans. By contrasting traditional and modern tools, we illustrate when and why 3D datasets may be preferable over 2D data, and vice versa, and how different methodologies can complement each other in comparative analyses of morphological function and evolution.

Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats.

Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed. Rather, models of discrete shifts between adaptive zones may better explain macroevolutionary dynamics across radiations. To investigate which of these processes underlie exceptional levels of morphological diversity during ecological diversification, we use modern phylogenetic tools and 3D geometric morphometric datasets to examine adaptive zone shifts in bat skull shape. Here we report that, while disparity was established early, bat skull evolution is best described by multiple adaptive zone shifts. Shifts are partially decoupled between the cranium and mandible, with cranial evolution more strongly driven by echolocation than diet. Phyllostomidae, a trophic adaptive radiation, exhibits more adaptive zone shifts than all other families combined. This pattern was potentially driven by ecological opportunity and facilitated by a shift to intermediate cranial shapes compared to oral-emitters and other nasal emitters.

Tongue-driven sonar beam steering by a lingual-echolocating fruit bat.

Animals enhance sensory acquisition from a specific direction by movements of head, ears, or eyes. As active sensing animals, echolocating bats also aim their directional sonar beam to selectively "illuminate" a confined volume of space, facilitating efficient information processing by reducing echo interference and clutter. Such sonar beam control is generally achieved by head movements or shape changes of the sound-emitting mouth or nose. However, lingual-echolocating Egyptian fruit bats, Rousettus aegyptiacus, which produce sound by clicking their tongue, can dramatically change beam direction at very short temporal intervals without visible morphological changes. The mechanism supporting this capability has remained a mystery. Here, we measured signals from free-flying Egyptian fruit bats and discovered a systematic angular sweep of beam focus across increasing frequency. This unusual signal structure has not been observed in other animals and cannot be explained by the conventional and widely-used "piston model" that describes the emission pattern of other bat species. Through modeling, we show that the observed beam features can be captured by an array of tongue-driven sound sources located along the side of the mouth, and that the sonar beam direction can be steered parsimoniously by inducing changes to the pattern of phase differences through moving tongue location. The effects are broadly similar to those found in a phased array-an engineering design widely found in human-made sonar systems that enables beam direction changes without changes in the physical transducer assembly. Our study reveals an intriguing parallel between biology and human engineering in solving problems in fundamentally similar ways.

A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity.

Primates represent one of the most species rich, wide ranging, and ecologically diverse clades of mammals. What major macroevolutionary factors have driven their diversification and contributed to the modern distribution of primate species remains widely debated. We employed phylogenetic comparative methods to examine the role of clade age and evolutionary rate heterogeneity in the modern distribution of species diversity of Primates. Primate diversification has accelerated since its origin, with decreased extinction leading to a shift to even higher evolutionary rates in the most species rich family (Cercopithecidae). Older primate clades tended to be more diverse, however a shift in evolutionary rate was necessary to adequately explain the imbalance in species diversity. Species richness was also poorly explained by geographic distribution, especially once clade age and evolutionary rate shifts were accounted for, and may relate instead to other ecological factors. The global distribution of primate species diversity appears to have been strongly impacted by heterogeneity in evolutionary rates.

Selection towards different adaptive optima drove the early diversification of locomotor phenotypes in the radiation of Neotropical geophagine cichlids.

BACKGROUND: Simpson envisaged a conceptual model of adaptive radiation in which lineages diversify into "adaptive zones" within a macroevolutionary adaptive landscape. However, only a handful of studies have empirically investigated this adaptive landscape and its consequences for our interpretation of the underlying mechanisms of phenotypic evolution. In fish radiations the evolution of locomotor phenotypes may represent an important dimension of ecomorphological diversification given the implications of locomotion for feeding and habitat use. Neotropical geophagine cichlids represent a newly identified adaptive radiation and provide a useful system for studying patterns of locomotor diversification and the implications of selective constraints on phenotypic divergence in general. RESULTS: We use multivariate ordination, models of phenotypic evolution and posterior predictive approaches to investigate the macroevolutionary adaptive landscape and test for evidence of early divergence of locomotor phenotypes in Geophagini. The evolution of locomotor phenotypes was characterized by selection towards at least two distinct adaptive peaks and the early divergence of modern morphological disparity. One adaptive peak included the benthic and epibenthic invertivores and was characterized by fishes with deep, laterally compressed bodies that optimize precise, slow-swimming manoeuvres. The second adaptive peak resulted from a shift in adaptive optima in the species-rich ram-feeding/rheophilic Crenicichla-Teleocichla clade and was characterized by species with streamlined bodies that optimize fast starts and rapid manoeuvres. Evolutionary models and posterior predictive approaches favoured an early shift to a new adaptive peak over decreasing rates of evolution as the underlying process driving the early divergence of locomotor phenotypes. CONCLUSIONS: The influence of multiple adaptive peaks on the divergence of locomotor phenotypes in Geophagini is compatible with the expectations of an ecologically driven adaptive radiation. This study confirms that the diversification of locomotor phenotypes represents an important dimension of phenotypic evolution in the geophagine adaptive radiation. It also suggests that the commonly observed early burst of phenotypic evolution during adaptive radiations may be better explained by the concentration of shifts to new adaptive peaks deep in the phylogeny rather than overall decreasing rates of evolution.

Testing for ancient adaptive radiations in neotropical cichlid fishes.

Most contemporary studies of adaptive radiation focus on relatively recent and geographically restricted clades. It is less clear whether diversification of ancient clades spanning entire continents is consistent with adaptive radiation. We used novel fossil calibrations to generate a chronogram of Neotropical cichlid fishes and to test whether patterns of lineage and morphological diversification are congruent with hypothesized adaptive radiations in South and Central America. We found that diversification in the Neotropical cichlid clade and the highly diverse tribe Geophagini was consistent with diversity-dependent, early bursts of divergence followed by decreased rates of lineage accumulation. South American Geophagini underwent early rapid differentiation in body shape, expanding into novel morphological space characterized by elongate-bodied predators. Divergence in head shape attributes associated with trophic specialization evolved under strong adaptive constraints in all Neotropical cichlid clades. The South American Cichlasomatini followed patterns consistent with constant rates of morphological divergence. Although morphological diversification in South American Heroini was limited, Eocene invasion of Central American habitats was followed by convergent diversification mirroring variation observed in Geophagini. Diversification in Neotropical cichlids was influenced by the early adaptive radiation of Geophagini, which potentially limited differentiation in other cichlid clades.

Testing of the effect of missing data estimation and distribution in morphometric multivariate data analyses.

Missing data are an unavoidable problem in biological data sets and the performance of missing data deletion and estimation techniques in morphometric data sets is poorly understood. Here, a novel method is used to measure the introduced error of multiple techniques on a representative sample. A large sample of extant crocodilian skulls was measured and analyzed with principal component analysis (PCA). Twenty-three different proportions of missing data were introduced into the data set, estimated, analyzed, and compared with the original result using Procrustes superimposition. Previous work investigating the effects of missing data input missing values randomly, a non-biological phenomenon. Here, missing data were introduced into the data set using three methodologies: purely at random, as a function of the Euclidean distance between respective measurements (simulating anatomical regions), and as a function of the portion of the sample occupied by each taxon (simulating unequal missing data in rare taxa). Gower's distance was found to be the best performing non-estimation method, and Bayesian PCA the best performing estimation method. Specimens of the taxa with small sample sizes and those most morphologically disparate had the highest estimation error. Distribution of missing data had a significant effect on the estimation error for almost all methods and proportions. Taxonomically biased missing data tended to show similar trends to random, but with higher error rates. Anatomically biased missing data showed a much greater deviation from random than the taxonomic bias, and with magnitudes dependent on the estimation method.

Guianacara dacrya, a new species from the rio Branco and Essequibo River drainages of the Guiana Shield (Perciformes: Cichlidae)

Describimos una especie nueva de Guianacara de las cuencas del río Essequibo y el río Branco en Guyana y el norte de Brasil. Guianacara dacrya, especie nueva, puede distinguirse de todos sus congéneres por la presencia de una barra infraorbital modificada y por la forma única del margen lateral de la placa dentada de la mandíbula faríngea inferior. Adicionalmente, Guianacara dacrya se distingue de G. stergiosi, G. owroewefi, G. sphenozona y G. geayi por poseer una barra medio-lateral fina, de G. cuyunii por poseer membranas branquistegales grises y de G. oelemariensis por poseer dos supraneurales. La especie nueva se distingue de la mayoría de sus congéneres por la presencia de manchas blancas en la porción espinosa de la aleta dorsal, la posición de la mancha medio-lateral, la presencia de filamentos en la aleta dorsal, anal y en algunos casos en la caudal, y de al menos las especies venezolanas por varias características morfométricas. Guianacara dacrya se conoce de las cuencas del ríos Essequibo, Takutu e Ireng en Guyana y posiblemente del río Uraricoera en la cuenca del río Branco en Brasil. Se presenta una clave de especies.

A new species of Guianacara is described from tributaries of the Essequibo River and the rio Branco in Guyana and northern Brazil. Guianacara dacrya, new species, can be diagnosed from all congeners by the possession of a unique infraorbital stripe and by the shape of the lateral margin of the lower pharyngeal jaw tooth plate. Guianacara dacrya can be further distinguished from G. geayi, G. owroewefi, G. sphenozona and G. stergiosi by the possession of a thin midlateral bar, from G. cuyunii by the possession of dusky branchiostegal membranes and from G. oelemariensis by the possession of two supraneurals. This species differs from most congeners by the presence of white spots on the spiny portion of the dorsal fin, the placement of the midlateral spot, the presence of filaments on the dorsal, anal and in rare cases the caudal-fin and from at least the Venezuelan species by several morphometric variables. Guianacara dacrya is known from the Essequibo, Takutu and Ireng River basins of Guyana and possibly from the rio Uraricoera in the rio Branco basin in Brazil. A key to the species is provided.