Reduced performance of prey targeting in pit vipers with contralaterally occluded infrared and visual senses

Both visual and infrared (IR) senses are utilized in prey targeting by pit vipers. Visual and IR inputs project to the contralateral optic tectum where they activate both multimodal and bimodal neurons. A series of ocular and pit organ occlusion experiments using the short-tailed pit viper (Gloydius brevicaudus) were conducted to investigate the role of visual and IR information during prey targeting. Compared with unoccluded controls, snakes with either both eyes or pit organs occluded performed more poorly in hunting prey although such subjects still captured prey on 75% of trials. Subjects with one eye and one pit occluded on the same side of the face performed as well as those with bilateral occlusion although these subjects showed a significant targeting angle bias toward the unoccluded side. Performance was significantly poorer when only a single eye or pit was available. Interestingly, when one eye and one pit organ were occluded on opposite sides of the face, performance was poorest, the snakes striking prey on no more than half the trials. These results indicate that, visual and infrared information are both effective in prey targeting in this species, although interference between the two modalities occurs if visual and IR information is restricted to opposite sides of the brain.     

Host and brood parasite coevolutionary interactions covary with comparative patterns of the avian visual system

In coevolutionary arms-races, reciprocal ecological interactions and their fitness impacts shape the course of phenotypic evolution. The classic example of avian host–brood parasite interactions selects for host recognition and rejection of increasingly mimetic foreign eggs. An essential component of perceptual mimicry is that parasitic eggs escape detection by host sensory systems, yet there is no direct evidence that the avian visual system covaries with parasitic egg recognition or mimicry. Here, we used eye size measurements collected from preserved museum specimens as a metric of the avian visual system for species involved in host–brood parasite interactions. We discovered that (i) hosts had smaller eyes compared with non-hosts, (ii) parasites had larger eyes compared with hosts before but not after phylogenetic corrections, perhaps owing to the limited number of independent evolutionary origins of obligate brood parasitism, (iii) egg rejection in hosts with non-mimetic parasitic eggs positively correlated with eye size, and (iv) eye size was positively associated with increased avian-perceived host–parasite eggshell similarity. These results imply that both host-use by parasites and anti-parasitic responses by hosts covary with a metric of the visual system across relevant bird species, providing comparative evidence for coevolutionary patterns of host and brood parasite sensory systems.     

Sex and Caste-Specific Variation in Compound Eye Morphology of Five Honeybee Species

Ranging from dwarfs to giants, the species of honeybees show remarkable differences in body size that have placed evolutionary constrains on the size of sensory organs and the brain. Colonies comprise three adult phenotypes, drones and two female castes, the reproductive queen and sterile workers. The phenotypes differ with respect to tasks and thus selection pressures which additionally constrain the shape of sensory systems. In a first step to explore the variability and interaction between species size-limitations and sex and caste-specific selection pressures in sensory and neural structures in honeybees, we compared eye size, ommatidia number and distribution of facet lens diameters in drones, queens and workers of five species (Apis andreniformis, A. florea, A. dorsata, A. mellifera, A. cerana). In these species, male and female eyes show a consistent sex-specific organization with respect to eye size and regional specialization of facet diameters. Drones possess distinctly enlarged eyes with large dorsal facets. Aside from these general patterns, we found signs of unique adaptations in eyes of A. florea and A. dorsata drones. In both species, drone eyes are disproportionately enlarged. In A. dorsata the increased eye size results from enlarged facets, a likely adaptation to crepuscular mating flights. In contrast, the relative enlargement of A. florea drone eyes results from an increase in ommatidia number, suggesting strong selection for high spatial resolution. Comparison of eye morphology and published mating flight times indicates a correlation between overall light sensitivity and species-specific mating flight times. The correlation suggests an important role of ambient light intensities in the regulation of species-specific mating flight times and the evolution of the visual system. Our study further deepens insights into visual adaptations within the genus Apis and opens up future perspectives for research to better understand the timing mechanisms and sensory physiology of mating related signals.     

Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae)

Hypotheses for the origin and maintenance of sexual size dimorphism (SSD) fall into three primary categories: (i) sexual selection on male size, (ii) fecundity selection on female size and (iii) ecological selection for gender‐specific niche divergence. We investigate the impact of these forces on SSD evolution in New World pitvipers (Crotalinae). We constructed a phylogeny from up to eight genes (seven mitochondrial, one nuclear) for 104 species of NW crotalines. We gathered morphological and ecological data for 82 species for comparative analyses. There is a strong signal of sexual selection on male size driving SSD, but less evidence for fecundity selection on female size across lineages. No support was found for allometric scaling of SSD (Rensch's rule), nor for directional selection for increasing male size (the Fairbairn–Preziosi hypothesis) in NW crotalines. Interestingly, arboreal lineages experience higher rates of SSD evolution and a pronounced shift to female‐biased dimorphism. This suggests that fecundity selection on arboreal females exaggerates ecologically mediated dimorphism, whereas sexual selection drives male size in terrestrial lineages. We find that increasing SSD in both directions (male‐ and female‐biased) decreases speciation rates. In NW crotalines, it appears that increasing magnitudes of ecologically mediated SSD reduce rates of speciation, as divergence accumulates within species among sexes, reducing adaptive divergence between populations leading to speciation.     

Macroevolution of arboreality in salamanders

Evolutionary theory predicts that selection in distinct microhabitats generates correlations between morphological and ecological traits, and may increase both phenotypic and taxonomic diversity. However, some microhabitats exert unique selective pressures that act as a restraining force on macroevolutionary patterns of diversification. In this study, we use phylogenetic comparative methods to investigate the evolutionary outcomes of inhabiting the arboreal microhabitat in salamanders. We find that arboreality has independently evolved at least five times in Caudata and has arisen primarily from terrestrial ancestors. However, the rate of transition from arboreality back to terrestriality is 24 times higher than the converse. This suggests that macroevolutionary trends in microhabitat use tend toward terrestriality over arboreality, which influences the extent to which use of the arboreal microhabitat proliferates. Morphologically, we find no evidence for an arboreal phenotype in overall body proportions or in foot shape, as variation in both traits overlaps broadly with species that utilize different microhabitats. However, both body shape and foot shape display reduced rates of phenotypic evolution in arboreal taxa, and evidence of morphological convergence among arboreal lineages is observed. Taken together, these patterns suggest that arboreality has played a unique role in the evolution of this family, providing neither an evolutionary opportunity, nor an evolutionary dead end.     

A functional analysis of compound eye evolution

New data on the phylogenetic relationships of various arthropod groups have spurred interesting attempts to reconstruct the evolution of arthropod nervous and visual systems. Some of the relevant new data are cell identities and developmental processes in the nervous and sensory systems, which is particularly useful for reconstructing the evolution of these systems. Here, we focus on the structure of compound eye ommatidia, and make an evolutionary analysis with functional arguments. We investigate possible routes of evolution that can be understood in terms of selection for improved visual function, and arrive at a number of conclusions that are discussed in the light of recent phylogenetic hypotheses. On the basis of ommatidial focusing structures and the arrangement of receptor cells we show that the evolution of compound eyes proceeded largely independently along at least two lineages from very primitive ancestors. A common ancestor of insects and crustaceans is likely to have had ommatidia with focusing crystalline cones, and colour and/or polarization vision. In contrast, the compound eyes in myriapods and chelicerates are likely to date back to ancestors with corneal lenses and probably without the ability to discriminate colour and polarization.     

Eye morphology in cathemeral lemurids and other mammals

The visual systems of cathemeral mammals are subject to selection pressures that are not encountered by strictly diurnal or nocturnal species. In particular, the cathemeral eye and retina must be able to function effectively across a broad range of ambient light intensities. This paper provides a review of the current state of knowledge regarding the visual anatomy of cathemeral primates, and presents an analysis of the influence of cathemerality on eye morphology in the genus Eulemur. Due to the mutual antagonism between most adaptations for increased visual acuity and sensitivity, cathemeral lemurs are expected to resemble other cathemeral mammals in having eye morphologies that are intermediate between those of diurnal and nocturnal close relatives. However, if lemurs only recently adopted cathemeral activity patterns, then cathemeral lemurids would be expected to demonstrate eye morphologies more comparable to those of nocturnal strepsirrhines. Both predictions were tested through a comparative study of relative cornea size in mammals. Intact eyes were collected from 147 specimens of 55 primate species, and relative corneal dimensions were compared to measurements taken from a large sample of non-primate mammals. These data reveal that the five extant species of the cathemeral genus Eulemur have relative cornea sizes intermediate between those of diurnal and nocturnal strepsirrhines. Moreover, all Eulemur species have relative cornea sizes that are comparable to those of cathemeral non-primate mammals and significantly smaller than those of nocturnal mammals. These results suggest that Eulemur species resemble other cathemeral mammals in having eyes that are adapted to function under variable environmental light levels. These results also suggest that cathemerality is a relatively ancient adaptation in Eulemur that was present in the last common ancestor of the genus (ca. 8-12 MYA).     

Behavioural examination of the infrared sensitivity of rattlesnakes (Crotalus atrox)

Pitvipers (Crotalinae) and boid snakes (Boidae) possess highly sensitive infrared (IR) receptors. The ability of these snakes to image IR radiation allows the assessment of the direction and distance of an IR source (such as warm-blooded prey) in the absence of visual cues. The aim of this study was to determine the behavioural threshold of snakes to an IR stimulus. A moving IR source of constant size and temperature was presented to rattlesnakes (Crotalus atrox) at various distances (10–160 cm) from their snout. The snakes’ responses were quantified by measuring distinct behavioural changes during stimulus presentation (head jerks, head fixed, freezing, rattling and tongue-flicking). The results revealed that C. atrox can detect an artificial IR stimulus resembling a mouse in temperature and size up to a distance of 100 cm, which corresponds to a radiation density of 3.35 × 10⁻³ mW/cm². These behavioural results reveal a 3.2 times higher sensitivity to IR radiation than earlier electrophysiological investigations.     

Pupil dilation and visual field in the piked dogfish, <Emphasis Type="Italic">Squalus acanthias</Emphasis>

The relatively large eye and pupil of the Piked Dogfish, Squalus acanthias, is visually arresting. However, knowledge of its basic visual characteristics lags far behind other areas in this generally well studied species. This study quantifies pupil dilation in a species that is naturally exposed to a broad range of light intensities and finds that the pupil area in the dark adapted state is 35.3% of the total eye area, an increase of 12.4% from the light adapted state. The anterior and posterior extents of the horizontal visual field are assessed and compared with both morphological and electrophysiological techniques and the results are integrated with the measured head yaw to derive the anterior convergence distance and blind area. The position of the eyes and the triangular, pointed snout of S. acanthias provides excellent anterior vision, which likely facilitates foraging upon its mobile prey.     

Morphological adaptations to arboreal habitats and heart position in species of the neotropical whipsnakes genus Chironius

The evolution of arboreality in snakes is accompanied by modifications that are remarkably similar across species. Gravity is one of the most important selective agents, and arboreal snakes present adaptations to circumvent the gradient of pressure, including modifications on heart position (HP) and body slenderness (BS). However, the degree to which different life‐history traits influence the cardiovascular system of snakes remains unclear. Here, we used an ecological and a phylogenetic approach to explore the relationship between habitat, HP, BS, and heart size (HS) in five species of the neotropical whipsnakes genus Chironius that occupy terrestrial, semiarboreal, and arboreal habits. Our ecological comparison indicated that the arboreal species have the most posterior‐positioned heart, the most slender body, and the smallest HS, whereas the terrestrial representative of the group exhibited the most anterior heart, the less flattened body, and the largest HS. After removing the phylogenetic effect, we found no difference in HP and BS between terrestrial and arboreal species. Habitat only differed when contrasting with HS. Body slenderness and HS were correlated with HP. Our results suggest that different restrictions, such as anatomical constraints, behavior, and phylogenetic inertia, may be important for the studied species.     

Anophthalmia and elongation of body appendages in cave scale worms (Annelida: Aphroditiformia)

This study addresses whether cave dwelling annelids exhibited similar reductive and constructive traits equally as strong as those of arthropods and vertebrates inhabiting caves. Known as troglomorphism, these adaptations bring about striking morphologies across invertebrates and vertebrates from both aquatic and terrestrial cave habitats, and include varying degrees of eye and pigmentation loss, as well as hypertrophy of body appendages and sensorial structures. Employing phylogenetic comparative methods and ancestral character reconstructions on a worldwide data set of a group of annelids, the scale worms (Aphroditiformia), we investigate the behavioural and morphological traits of species living in marine caves in comparison with those species living outside caves. Our work demonstrated that cave scale worms respond similar to arthropods in cave environments, showing a significant elongation of sensory parapodial cirri, while lacking eyes and pigmentation. However, whereas elongation of sensory appendages likely occurred in correlation to cave colonization, eyes were plausibly lost in correlation with specialization and colonization of deep‐sea habitats.     

Ecological constraints on sensory systems: compound eye size in Daphnia is reduced by resource limitation

Eye size is an indicator of visual capability, and macroevolutionary patterns reveal that taxa inhabiting dim environments have larger eyes than taxa from bright environments. This suggests that the light environment is a key driver of variation in eye size. Yet other factors not directly linked with visual tasks (i.e., non-sensory factors) may influence eye size. We sought to jointly investigate the roles of sensory (light) and non-sensory factors (food) in determining eye size and ask whether non-sensory factors could constrain visual capabilities. We tested environmental influences on eye size in four species of the freshwater crustacean Daphnia, crossing bright and dim light levels with high and low resource levels. We measured absolute eye size and eye size relative to body size in early and late adulthood. In general, Daphnia reared on low resources had smaller eyes, both absolutely and relatively. In contrast to the dominant macroevolutionary pattern, phenotypic plasticity in response to light was rarely significant. These patterns of phenotypic plasticity were true for overall diameter of the eye and the diameter of individual facets. We conclude that non-sensory environmental factors can influence sensory systems, and in particular, that resource availability may be an important constraint on visual capability.     

Sexual selection, natural selection and copulatory patterns in male primates.

Complex copulatory patterns, involving multiple brief intromissions or prolonged single intromissions (PI) occur most frequently among primate species in which females mate with a number of partners (multimale and dispersed mating systems). However, the PI pattern is also confined almost exclusively to arboreal primates - to either smaller-bodied, cryptic, nocturnal species or much larger diurnal forms. Predation pressures may have limited the evolution of the PI pattern, particularly where small-bodied diurnal primates or terrestrial forms are concerned. The available evidence indicates that both sexual selection and natural selection may have influenced the evolution of copulatory patterns.     

Primate origins: Lessons from a neotropical marsupial

The didelphid Caluromys shows evolutionary convergence towards prosimians in having a relatively large brain, large eyes, small litters, slow development, and agile locomotion. The selection pressures that favored the emergence of primate-like traits in Caluromys from a generalized didelphid ancestor may be analogous to the selection pressures favoring the initial divergence of primates from a primitive nonprimate ancestor, and thus Caluromys provides an independent test of the arboreal hypothesis (Smith: Annual Report of the Board of Regents of the Smithsonian Institution 1912:553–572, 1913), the visual predation hypothesis (Cartmill: The Functional and Evolutionary Biology of Primates, pp. 97–122, 1972), and the angiosperm exploitation hypothesis (Sussman: American Journal of Primatology, in press) of primate origins. Quantitative data on free-ranging C. derbianus in Costa Rica demonstrate that it is highly arboreal, uses visually directed predation to capture arthropod prey, and makes extensive use of terminal branch foraging, where it feeds on small angiosperm products. These observations are consistent with predictions from each model of primate origins, thus suggesting that the hypotheses are not mutually exclusive but are interdependent. The initial divergence of primates probably involved exploitation of the rich angiosperm products and associated insects found in fine terminal branches; visually directed predation may have evolved as an efficient method of insect capture in the terminal branch milieu.     

Comparative histomorphology of intrinsic vibrissa musculature among primates: implications for the evolution of sensory ecology and “face touch”

Macrovibrissae are specialized tactile sensory hairs present in most mammalian orders, used in maxillary mechanoreception or “face touch.” Some mammals have highly organized vibrissae and are able to “whisk” them. Movement of vibrissae is influenced by intrinsic vibrissa musculature, striated muscle bands that attach directly to the vibrissa capsule. It is unclear if primates have organized vibrissae or intrinsic vibrissa musculature and it is uncertain if they can move their vibrissae. The present study used histomorphological techniques to compare vibrissae among 19 primates and seven non‐primate mammalian taxa. Upper lips of these mammals were sectioned and processed for histochemical analysis. While controlling for phylogenetic effects the following hypotheses were tested: 1) mammals with well‐organized vibrissae possess intrinsic vibrissa musculature and 2) intrinsic vibrissa musculature is best developed in nocturnal, arboreal taxa. Our qualitative analyses show that only arboreal, nocturnal prosimians possess intrinsic musculature. Not all taxa that possessed organized vibrissae had intrinsic vibrissa musculature. Phylogenetic comparative analyses revealed a 70% probability that stem mammals, primates, and haplorhines possessed intrinsic vibrissa musculature and well‐organized vibrissae. These two traits most likely coevolved according to a discrete phylogenetic analysis. These results indicate that nocturnal, arboreal primates have the potential to more actively use their vibrissae in spatial recognition and navigation tasks than diurnal, more terrestrial species, but there is a clear phylogenetic signal involved in the evolution of primate vibrissae and “face touch.” Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Temporal properties of the lens eyes of the box jellyfish Tripedalia cystophora

Box jellyfish (Cubomedusae) are visually orientating animals which posses a total of 24 eyes of 4 morphological types; 2 pigment cup eyes (pit eye and slit eye) and 2 lens eyes [upper lens-eye (ule) and lower lens-eye (lle)]. In this study, we use electroretinograms (ERGs) to explore temporal properties of the two lens eyes. We find that the ERG of both lens eyes are complex and using sinusoidal flicker stimuli we find that both lens eyes have slow temporal resolution. The average flicker fusion frequency (FFF) was found to be approximately 10 Hz for the ule and 8 Hz for the lle. Differences in the FFF and response patterns between the two lens eyes suggest that the ule and lle filter information differently in the temporal domain and thus are tuned to perform different visual tasks. The data collected in this study support the idea that the visual system of box jellyfish is a collection of special purpose eyes.     

Language, Handedness, and Primate Brains: Did the Australopithecines Sign?

Evidence from comparative primate neuroanatomy, archaeology, and studies of vocalization systems of nonhuman primates suggests that human vocal language has a long evolutionary history and that there is continuity between our early primate ancestors' call systems and human speech. Old World monkeys exhibit cerebral asymmetries similar to those that appear related to human language. If arboreal monkeylike ancestors of humans were also characterized by cerebral asymmetry, then the fundamental asymmetry that forms the neurological substrate for human language may have been established through selection for simple "discrete" call systems in an arboreal habitat and would have occurred much longer ago than previously thought. The eventual shift from an arboreal to a terrestrial habitat was accompanied by increased complexity ("gradation") of vocal communication systems. The archaeological record of tools suggests that communication systems became still more complex under the selective pressures that led to bipedalism and that language had been selected for by the time that bipedalism was achieved. Contrary to the gestural hypothesis, right-handedness (which could not have preceded freeing of the hands) succeeded speech and may have been due to selective pressures for increased complexity of communication, causing a Field Effect upon the brain. [australopithecine, cerebral asymmetry, language, primate brains, right-handedness]     

Preferred temperature correlates with evaporative water loss in hylid frogs from northern Australia

We measured temperature preferences of 12 species of hylid frogs (Litoria and Cyclorana) from northern Australia in a laboratory thermal gradient. These species represented a range of ecological habitat use (aquatic, terrestrial, arboreal), adult body size (0.5-60 g), and cutaneous resistance to water loss (Rc=0.6-63.1 s cm-1). We found significant differences among species in selected skin temperature and gradient temperature but not in the variances of these measures (an index of precision of temperature selection). The species' differences correlated significantly with cutaneous resistance to water loss, with more-resistant frogs selecting higher skin and substrate temperatures in the thermal gradient, even after phylogenetic relationships are taken into account. Because cutaneous resistance to water loss also correlates with ecological habit (arboreal>terrestrial>aquatic), we suggest that their higher resistance to water loss allows arboreal and terrestrial species better ability to tolerate high temperatures, where growth or locomotory speed may be higher, without the associated risk of desiccation.     

Rhodopsin Molecular Evolution in Mammals Inhabiting Low Light Environments

The ecological radiation of mammals to inhabit a variety of light environments is largely attributed to adaptive changes in their visual systems. Visual capabilities are conferred by anatomical features of the eyes as well as the combination and properties of their constituent light sensitive pigments. To test whether evolutionary switches to different niches characterized by dim-light conditions coincided with molecular adaptation of the rod pigment rhodopsin, we sequenced the rhodopsin gene in twenty-two mammals including several bats and subterranean mole-rats. We compared these to thirty-seven published mammal rhodopsin sequences, from species with divergent visual ecologies, including nocturnal, diurnal and aquatic groups. All taxa possessed an intact functional rhodopsin; however, phylogenetic tree reconstruction recovered a gene tree in which rodents were not monophyletic, and also in which echolocating bats formed a monophyletic group. These conflicts with the species tree appear to stem from accelerated evolution in these groups, both of which inhabit low light environments. Selection tests confirmed divergent selection pressures in the clades of subterranean rodents and bats, as well as in marine mammals that live in turbid conditions. We also found evidence of divergent selection pressures among groups of bats with different sensory modalities based on vision and echolocation. Sliding window analyses suggest most changes occur in transmembrane domains, particularly obvious within the pinnipeds; however, we found no obvious pattern between photopic niche and predicted spectral sensitivity based on known critical amino acids. This study indicates that the independent evolution of rhodopsin vision in ecologically specialised groups of mammals has involved molecular evolution at the sequence level, though such changes might not mediate spectral sensitivity directly.