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Sensory organs must develop alongside the skull within which they are largely encased, and this relationship can manifest as the skull constraining the organs, organs constraining the skull, or organs constraining one another in relative size. How this interplay between sensory organs and the developing skull plays out during the evolution of sensory diversity; however, remains unknown. Here, we examine the developmental sequence of the cochlea, the organ responsible for hearing and echolocation, in species with distinct diet and echolocation types within the ecologically diverse bat super-family Noctilionoidea. We found the size and shape of the cochlea largely correlates with skull size, with exceptions of Pteronotus parnellii, whose high duty cycle echolocation (nearly constant emission of sound pulses during their echolocation process allowing for detailed information gathering, also called constant frequency echolocation) corresponds to a larger cochlear and basal turn, and Monophyllus redmani, a small-bodied nectarivorous bat, for which interactions with other sensory organs restrict cochlea size. Our findings support the existence of developmental constraints, suggesting that both developmental and anatomical factors may act synergistically during the development of sensory systems in noctilionoid bats., (© 2023 American Association for Anatomy.)

AbstractWith diverse mechanical and sensory functions, the vertebrate cranium is a complex anatomical structure whose shifts between modularity and integration, especially in mechanical function, have been implicated in adaptive diversification. Yet how mechanical and sensory systems and their functions coevolve, as well as how their interrelationship contributes to phenotypic disparity, remain largely unexplored. To examine the modularity, integration, and evolutionary rates of sensory and mechanical structures within the head, we analyzed hard and soft tissue scans from ecologically diverse bats in the superfamily Noctilionoidea, a clade that ranges from insectivores and carnivores to frugivores and nectarivores. We identified eight regions that evolved in a coordinated fashion, thus recognizable as evolutionary modules: five associated with bite force and three linked to olfactory, visual, and auditory systems. Interrelationships among these modules differ between Neotropical leaf-nosed bats (family Phyllostomidae) and other noctilionoids. Consistent with the hypothesis that dietary transitions begin with changes in the capacity to detect novel food items followed by adaptations to process them, peak rates of sensory module evolution predate those of some mechanical modules. We propose that the coevolution of structures influencing bite force, olfaction, vision, and hearing constituted a structural opportunity that allowed the phyllostomid ancestor to take advantage of existing ecological opportunities and contributed to the clade's remarkable radiation.

The relative contributions of adaptation and genetic drift to morphological diversification of the skulls of echolocating mammals were investigated using two horseshoe bat species, Rhinolophus simulator and R. cf. simulator , as test cases. We used 3D geometric morphometrics to compare the shapes of skulls of the two lineages collected at various localities in southern Africa. Size and shape variation was predominantly attributed to selective forces; the between-population variance ( B ) was not proportional to the within-population variance ( W ). Modularity was evident in the crania of R. simulator but absent in the crania of R. cf. simulator and the mandibles of both species. The skulls of the two lineages thus appeared to be under different selection pressures, despite the overlap in their distributions. Difference in the crania of R. cf. simulator was centered largely on the nasal dome region of R. cf. simulator but on the cranium and mandibles of R. simulator . It is likely that the size and shape of the nasal dome, which acts as a frequency-dependent acoustic horn, is more crucial in R. cf. simulator than in R. simulator because of the higher echolocation frequencies used by R. cf. simulator . A larger nasal dome in R. cf. simulator would allow the emission of higher intensity pulses, resulting in comparable detection distances to that of R. simulator . In contrast, selection pressure is probably more pronounced on the mandibles and cranium of R. simulator to compensate for the loss in bite force because of its elongated rostrum. The predominance of selection probably reflects the stringent association between environment and the optimal functioning of phenotypic characters associated with echolocation and feeding in bats., Competing Interests: The authors declare no competing interests., (© 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

The role of mechanical morphologies in the exploitation of novel niche space is well characterized; however, the role of sensory structures in unlocking new niches is less clear. Here, we investigate the relationship between the evolution of sensory structures and diet during the radiation of noctilionoid bats. With a broad range of foraging ecologies and a well-supported phylogeny, noctilionoids constitute an ideal group for studying this relationship. We used diffusible iodine-based contrast enhanced computed tomography scans of 44 noctilionoid species to analyze relationships between the relative volumes of three sensory structures (olfactory bulbs, orbits, and cochleae) and diet. We found a positive relationship between frugivory and both olfactory and orbit size. However, we also found a negative relationship between nectarivory and cochlea size. Ancestral state estimates suggest that larger orbits and olfactory bulbs were present in the common ancestor of family Phyllostomidae, but not in other noctilionoid. This constellation of traits indicates a shift toward omnivory at the base of Phyllostomidae, predating their radiation into an exceptionally broad range of dietary niches. This is consistent with a scenario in which changes in sensory systems associated with foraging and feeding set the stage for subsequent morphological modification and diversification., (© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.)

Geographic variation in sensory traits is usually influenced by adaptive processes because these traits are involved in crucial life-history aspects including orientation, communication, lineage recognition and mate choice. Studying this variation can therefore provide insights into lineage diversification. According to the Sensory Drive Hypothesis, lineage diversification may be driven by adaptation of sensory systems to local environments. It predicts that acoustic signals vary in association with local climatic conditions so that atmospheric attenuation is minimized and transmission of the signals maximized. To test this prediction, we investigated the influence of climatic factors (specifically relative humidity and temperature) on geographic variation in the resting frequencies of the echolocation pulses of Geoffroy's horseshoe bat, Rhinolophus clivosus. If the evolution of phenotypic variation in this lineage tracks climate variation, human induced climate change may lead to decreases in detection volumes and a reduction in foraging efficiency. A complex non-linear interaction between relative humidity and temperature affects atmospheric attenuation of sound and principal components composed of these correlated variables were, therefore, used in a linear mixed effects model to assess their contribution to observed variation in resting frequencies. A principal component composed predominantly of mean annual temperature (factor loading of -0.8455) significantly explained a proportion of the variation in resting frequency across sites (P < 0.05). Specifically, at higher relative humidity (around 60%) prevalent across the distribution of R. clivosus, increasing temperature had a strong negative effect on resting frequency. Climatic factors thus strongly influence acoustic signal divergence in this lineage, supporting the prediction of the Sensory Drive Hypothesis. The predicted future increase in temperature due to climate change is likely to decrease the detection volume in echolocating bats and adversely impact their foraging efficiency.

Natural selection and drift can act on populations individually, simultaneously or in tandem and our understanding of phenotypic divergence depends on our ability to recognize the contribution of each. According to the quantitative theory of evolution, if an organism has diversified through neutral evolutionary processes (mutation and drift), variation of phenotypic characteristics between different geographic localities ( B ) should be directly proportional to the variation within localities ( W ), that is, B  ∝  W . Significant deviations from this null model imply that non-neutral forces such as natural selection are acting on a phenotype. We investigated the relative contributions of drift and selection to intraspecific diversity using southern African horseshoe bats as a test case. We characterized phenotypic diversity across the distributional range of Rhinolophus simulator ( n =  101) and Rhinolophus swinnyi ( n =  125) using several traits associated with flight and echolocation. Our results suggest that geographic variation in both species was predominantly caused by disruptive natural selection ( B was not directly proportional to W ). Evidence for correlated selection (co-selection) among traits further confirmed that our results were not compatible with drift. Selection rather than drift is likely the predominant evolutionary process shaping intraspecific variation in traits that strongly impact fitness.

Despite many studies illustrating the perils of utilising mitochondrial DNA in phylogenetic studies, it remains one of the most widely used genetic markers for this purpose. Over the last decade, nuclear introns have been proposed as alternative markers for phylogenetic reconstruction. However, the resolution capabilities of mtDNA and nuclear introns have rarely been quantified and compared. In the current study we generated a novel ∼5kb dataset comprising six nuclear introns and a mtDNA fragment. We assessed the relative resolution capabilities of the six intronic fragments with respect to each other, when used in various combinations together, and when compared to the traditionally used mtDNA. We focused on a major clade in the horseshoe bat family (Afro-Palaearctic clade; Rhinolophidae) as our case study. This old, widely distributed and speciose group contains a high level of conserved morphology. This morphological stasis renders the reconstruction of the phylogeny of this group with traditional morphological characters complex. We sampled multiple individuals per species to represent their geographic distributions as best as possible (122 individuals, 24 species, 68 localities). We reconstructed the species phylogeny using several complementary methods (partitioned Maximum Likelihood and Bayesian and Bayesian multispecies-coalescent) and made inferences based on consensus across these methods. We computed pairwise comparisons based on Robinson-Foulds tree distance metric between all Bayesian topologies generated (27,000) for every gene(s) and visualised the tree space using multidimensional scaling (MDS) plots. Using our supported species phylogeny we estimated the ancestral state of key traits of interest within this group, e.g. echolocation peak frequency which has been implicated in speciation. Our results revealed many potential cryptic species within this group, even in taxa where this was not suspected a priori and also found evidence for mtDNA introgression. We demonstrated that by using just two introns one can recover a better supported species tree than when using the mtDNA alone, despite the shorter overall length of the combined introns. Additionally, when combining any single intron with mtDNA, we showed that the result is highly similar to the mtDNA gene tree and far from the true species tree and therefore this approach should be avoided. We caution against the indiscriminate use of mtDNA in phylogenetic studies and advocate for pilot studies to select nuclear introns. The selection of marker type and number is a crucial step that is best based on critical examination of preliminary or previously published data. Based on our findings and previous publications, we recommend the following markers to recover phylogenetic relationships between recently diverged taxa (<20 My) in bats and other mammals: ACOX2, COPS7A, BGN, ROGDI and STAT5A., (Copyright © 2016 Elsevier Inc. All rights reserved.)

Geographic variation can be an indicator of still poorly understood evolutionary processes such as adaptation and drift. Sensory systems used in communication play a key role in mate choice and species recognition. Habitat-mediated (i.e. adaptive) differences in communication signals may therefore lead to diversification. We investigated geographic variation in echolocation calls of African horseshoe bats, Rhinolophus simulator and R. swinnyi in the context of two adaptive hypotheses: 1) James' Rule and 2) the Sensory Drive Hypothesis. According to James' Rule body-size should vary in response to relative humidity and temperature so that divergence in call frequency may therefore be the result of climate-mediated variation in body size because of the correlation between body size and call frequency. The Sensory Drive Hypothesis proposes that call frequency is a response to climate-induced differences in atmospheric attenuation and predicts that increases in atmospheric attenuation selects for calls of lower frequency. We measured the morphology and resting call frequency (RF) of 111 R. simulator and 126 R. swinnyi individuals across their distributional range to test the above hypotheses. Contrary to the prediction of James' Rule, divergence in body size could not explain the variation in RF. Instead, acoustic divergence in RF was best predicted by latitude, geography and climate-induced differences in atmospheric attenuation, as predicted by the Sensory Drive Hypothesis. Although variation in RF was strongly influenced by temperature and humidity, other climatic variables (associated with latitude and altitude) as well as drift (as suggested by a positive correlation between call variation and geographic distance, especially in R. simulator) may also play an important role.

Avian influenza viruses (AIVs) are pathogens of global concern, but there has been little previous research on avian influenza in southern Africa and almost nothing is known about the dynamics of AIVs in the region. We counted, captured and sampled birds regularly at five sites, two in South Africa (Barberspan and Strandfontein) and one in each of Botswana (Lake Ngami), Mozambique (Lake Chuali) and Zimbabwe (Lakes Manyame and Chivero) between March 2007 and May 2009. The South African and Zimbabwean sites were visited every 2 months and the sites in Botswana and Mozambique every 4 months. During each visit we undertook 5-7 days of standardised bird counts followed by 5-10 days of capturing and sampling water-associated birds. We sampled 4,977 birds of 165 different species and completed 2,503 half-hour point counts. We found 125 positive rRT-PCR cases of avian influenza across all sites. Two viruses (H1N8 and H3N8) were isolated and additional H5, H6 and H7 strains were identified. We did not positively identify any highly pathogenic H5N1. Overall viral prevalence (2.51%) was similar to the lower range of European values, considerable spatial and temporal variation occurred in viral prevalence, and there was no detectable influence of the annual influx of Palearctic migrants. Although waterbirds appear to be the primary viral carriers, passerines may link wild birds and poultry. While influenza cycles are probably driven by the bird movements that result from rainfall patterns, the epidemiology of avian influenza in wild birds in the subregion is complex and there appears to be the possibility for viral transmission throughout the year.