Sharlene E. Santana

Morphological innovation, diversification and invasion of a new adaptive zone

How ecological opportunity relates to diversification is a central question in evolutionary biology. However, there are few empirical examples of how ecological opportunity and morphological innovation open new adaptive zones, and promote diversification. We analyse data on diet, skull morphology and bite performance, and relate these traits to diversification rates throughout the evolutionary history of an ecologically diverse family of mammals (Chiroptera: Phyllostomidae). We found a significant increase in diversification rate driven by increased speciation at the most recent common ancestor of the predominantly frugivorous subfamily Stenodermatinae. The evolution of diet was associated with skull morphology, and morphology was tightly coupled with biting performance, linking phenotype to new niches through performance. Following the increase in speciation rate, the rate of morphological evolution slowed, while the rate of evolution in diet increased. This pattern suggests that morphology stabilized, and niches within the new adaptive zone of frugivory were filled rapidly, after the evolution of a new cranial phenotype that resulted in a certain level of mechanical efficiency. The tree-wide speciation rate increased non linearly with a more frugivorous diet, and was highest at measures of skull morphology associated with morphological extremes, including the most derived Stenodermatines. These results show that a novel stenodermatine skull phenotype played a central role in the evolution of frugivory and increasing speciation within phyllostomids.

Adaptive evolution of facial colour patterns in Neotropical primates

The rich diversity of primate faces has interested naturalists for over a century. Researchers have long proposed that social behaviours have shaped the evolution of primate facial diversity. However, the primate face constitutes a unique structure where the diverse and potentially competing functions of communication, ecology and physiology intersect, and the major determinants of facial diversity remain poorly understood. Here, we provide the first evidence for an adaptive role of facial colour patterns and pigmentation within Neotropical primates. Consistent with the hypothesis that facial patterns function in communication and species recognition, we find that species living in smaller groups and in sympatry with a higher number of congener species have evolved more complex patterns of facial colour. The evolution of facial pigmentation and hair length is linked to ecological factors, and ecogeographical rules related to UV radiation and thermoregulation are met by some facial regions. Our results demonstrate the interaction of behavioural and ecological factors in shaping one of the most outstanding facial diversities of any mammalian lineage.

Predicting bite force in mammals: two-dimensional versus three-dimensional lever models.

SUMMARY Bite force is a measure of whole-organism performance that is often used to investigate the relationships between performance, morphology and fitness. When in vivo measurements of bite force are unavailable, researchers often turn to lever models to predict bite forces. This study demonstrates that bite force predictions based on two-dimensional (2-D) lever models can be improved by including three-dimensional (3-D) geometry and realistic physiological cross-sectional areas derived from dissections. Widely used, the 2-D method does a reasonable job of predicting bite force. However, it does so by over predicting physiological cross-sectional areas for the masseter and pterygoid muscles and under predicting physiological cross-sectional areas for the temporalis muscle. We found that lever models that include the three dimensional structure of the skull and mandible and physiological cross-sectional areas calculated from dissected muscles provide the best predictions of bite force. Models that accurately represent the biting mechanics strengthen our understanding of which variables are functionally relevant and how they are relevant to feeding performance.

Connecting behaviour and performance: the evolution of biting behaviour and bite performance in bats

Variation in behaviour, performance and ecology are traditionally associated with variation in morphology. A neglected part of this ecomorphological paradigm is the interaction between behaviour and performance, the ability to carry out tasks that impact fitness. Here we investigate the relationship between biting behaviour and performance (bite force) among 20 species of ecologically diverse bats. We studied the patterns of evolution of plasticity in biting behaviour and bite force, and reconstructed ancestral states for behaviour and its plasticity. Both behavioural and performance plasticity exhibited accelerating evolution over time, and periods of rapid evolution coincided with major dietary shifts from insect‐feeding to plant‐feeding. We found a significant, positive correlation between behavioural plasticity and bite force. Bats modulated their performance by changing their biting behaviour to maximize bite force when feeding on hard foods. The ancestor of phyllostomids was likely a generalist characterized by high behavioural plasticity, a condition that also evolved in specialized frugivores and potentially contributed to their diversification.

DIETARY HARDNESS, LOADING BEHAVIOR, AND THE EVOLUTION OF SKULL FORM IN BATS

The morphology and biomechanics of the vertebrate skull reflect the physical properties of diet and behaviors used in food acquisition and processing. We use phyllostomid bats, the most diverse mammalian dietary radiation, to investigate if and how changes in dietary hardness and loading behaviors during feeding shaped the evolution of skull morphology and biomechanics. When selective regimes of food hardness are modeled, we found that species consuming harder foods have evolved skull shapes that allow for more efficient bite force production. These species have shorter skulls and a greater reliance on the temporalis muscle, both of which contribute to a higher mechanical advantage at an intermediate gape angle. The evolution of cranial morphology and biomechanics also appears to be related to loading behaviors. Evolutionary changes in skull shape and the relative role of the temporalis and masseter in generating bite force are correlated with changes in the use of torsional and bending loading behaviors. Functional equivalence appears to have evolved independently among three lineages of species that feed on liquids and are not obviously morphologically similar. These trends in cranial morphology and biomechanics provide insights into behavioral and ecological factors shaping the skull of a trophically diverse clade of mammals.

A phylogenetic analysis of armored scale insects (Hemiptera: Diaspididae), based upon nuclear, mitochondrial, and endosymbiont gene sequences

Armored scale insects (Hemiptera: Diaspididae) are among the most invasive insects in the world. They have unusual genetic systems, including diverse types of paternal genome elimination (PGE) and parthenogenesis. Intimate relationships with their host plants and bacterial endosymbionts make them potentially important subjects for the study of co-evolution. Here, we expand upon recent phylogenetic work (Morse and Normark, 2006) by analyzing armored scale and endosymbiont DNA sequences from 125 species of armored scale insect, represented by 253 samples and eight outgroup species. We used fragments of four different gene regions: the nuclear protein-coding gene Elongation Factor 1α (EF1α), the large ribosomal subunit (28S) rDNA, a mitochondrial region spanning parts of cytochrome oxidase I (COI) and cytochrome oxidase II (COII), and the small ribosomal subunit (16S) rDNA from the primary bacterial endosymbiont Uzinura diaspidicola. Maximum likelihood, and Bayesian analyses were performed producing highly congruent topological results. A comparison of two datasets, one with and one without missing data, found that missing data had little effect on topology. Our results broadly corroborate several major features of the existing classification, although we do not find any of the subfamilies, tribes or subtribes to be monophyletic as currently constituted. Using ancestral state reconstruction we estimate that the ancestral armored scale had the late PGE sex system, and it may as well have been pupillarial, though results differed between reconstruction methods. These results highlight the need for a complete revision of this family, and provide the groundwork for future taxonomic work in armored scale insects.

Does nasal echolocation influence the modularity of the mammal skull

In vertebrates, changes in cranial modularity can evolve rapidly in response to selection. However, mammals have apparently maintained their pattern of cranial integration throughout their evolutionary history and across tremendous morphological and ecological diversity. Here, we use phylogenetic, geometric morphometric and comparative analyses to test the hypothesis that the modularity of the mammalian skull has been remodelled in rhinolophid bats due to the novel and critical function of the nasal cavity in echolocation. We predicted that nasal echolocation has resulted in the evolution of a third cranial module, the ‘nasal dome’, in addition to the braincase and rostrum modules, which are conserved across mammals. We also test for similarities in the evolution of skull shape in relation to habitat across rhinolophids. We find that, despite broad variation in the shape of the nasal dome, the integration of the rhinolophid skull is highly consistent with conserved patterns of modularity found in other mammals. Across their broad geographical distribution, cranial shape in rhinolophids follows two major divisions that could reflect adaptations to dietary and environmental differences in African versus South Asian distributions. Our results highlight the potential of a relatively simple modular template to generate broad morphological and functional variation in mammals.

Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines

The faces of Old World monkeys and apes (Catarrhini) exhibit every possible hue in the spectrum of mammal colours. Animal colouration experiences selection for communication, physiology and ecology; however, the relative importance of these factors in producing facial diversity in catarrhines is not known. Here we adopt a comparative approach to test whether facial traits have evolved in tandem with social, geographic and ecological pressures across four catarrhine radiations. Our analyses reveal the underlying correlates of two major axes in the evolution of facial diversity. Facial colour patterns are linked to social factors, such that gregarious and highly sympatric species have evolved more colours in their faces. Facial pigmentation tends to be dominated by ecological factors, and species living in tropical, densely forested and humid habitats in Africa have evolved darker faces. Thus, both sociality and ecology have played a role in producing the highest diversity of faces within mammals.

All you can eat: high performance capacity and plasticity in the common big-eared bat, Micronycteris microtis (Chiroptera: Phyllostomidae).

Ecological specialization and resource partitioning are expected to be particularly high in the species-rich communities of tropical vertebrates, yet many species have broader ecological niches than expected. In Neotropical ecosystems, Neotropical leaf-nosed bats (Phyllostomidae) are one of the most ecologically and functionally diverse vertebrate clades. Resource partitioning in phyllostomids might be achieved through differences in the ability to find and process food. We selected Micronycteris microtis, a very small (5–7 g) animalivorous phyllostomid, to explore whether broad resource use is associated with specific morphological, behavioral and performance traits within the phyllostomid radiation. We documented processing of natural prey and measured bite force in free-ranging M. microtis and other sympatric phyllostomids. We found that M. microtis had a remarkably broad diet for prey size and hardness. For the first time, we also report the consumption of vertebrates (lizards), which makes M. microtis the smallest carnivorous bat reported to date. Compared to other phyllostomids, M. microtis had the highest bite force for its size and cranial shape and high performance plasticity. Bite force and cranial shape appear to have evolved rapidly in the M. microtis lineage. High performance capacity and high efficiency in finding motionless prey might be key traits that allow M. microtis, and perhaps other species, to successfully co-exist with other gleaning bats.

Go big or go fish: morphological specializations in carnivorous bats.

Specialized carnivory is relatively uncommon across mammals, and bats constitute one of the few groups in which this diet has evolved multiple times. While size and morphological adaptations for carnivory have been identified in other taxa, it is unclear what phenotypic traits characterize the relatively recent evolution of carnivory in bats. To address this gap, we apply geometric morphometric and phylogenetic comparative analyses to elucidate which characters are associated with ecological divergence of carnivorous bats from insectivorous ancestors, and if there is morphological convergence among independent origins of carnivory within bats, and with other carnivorous mammals. We find that carnivorous bats are larger and converged to occupy a subset of the insectivorous morphospace, characterized by skull shapes that enhance bite force at relatively wide gapes. Piscivorous bats are morphologically distinct, with cranial shapes that enable high bite force at narrow gapes, which is necessary for processing fish prey. All animal-eating species exhibit positive allometry in rostrum elongation with respect to skull size, which could allow larger bats to take relatively larger prey. The skull shapes of carnivorous bats share similarities with generalized carnivorans, but tend to be more suited for increased bite force production at the expense of gape, when compared with specialized carnivorans.