Ultraviolet-sensitive vision in long-lived birds

Long-term exposure to ultraviolet (UV) light generates substantial damage, and in mammals, visual sensitivity to UV is restricted to short-lived diurnal rodents and certain marsupials. In humans, the cornea and lens absorb all UV-A and most of the terrestrial UV-B radiation, preventing the reactive and damaging shorter wavelengths from reaching the retina. This is not the case in certain species of long-lived diurnal birds, which possess UV-sensitive (UVS) visual pigments, maximally sensitive below 400 nm. The Order Psittaciformes contains some of the longest lived bird species, and the two species examined so far have been shown to possess UVS pigments. The objective of this study was to investigate the prevalence of UVS pigments across long-lived parrots, macaws and cockatoos, and therefore assess whether they need to cope with the accumulated effects of exposure to UV-A and UV-B over a long period of time. Sequences from the SWS1 opsin gene revealed that all 14 species investigated possess a key substitution that has been shown to determine a UVS pigment. Furthermore, in vitro regeneration data, and lens transparency, corroborate the molecular findings of UV sensitivity. Our findings thus support the claim that the Psittaciformes are the only avian Order in which UVS pigments are ubiquitous, and indicate that these long-lived birds have UV sensitivity, despite the risks of photodamage.     

Nestling coloration is adjusted to parent visual performance in altricial birds irrespective of assumptions on vision system for Laniidae and owls,a reply to Renoult et al.

We have recently published support to the hypothesis that visual systems of parents could affect nestling detectability and, consequently, influences the evolution of nestling colour designs in altricial birds. We provided comparative evidence of an adjustment of nestling colour designs to the visual system of parents that we have found in a comparative study on 22 altricial bird species. In this issue, however, Renoult et al. ( J. Evol. Biol., 2009 ) question some of the assumptions and statistical approaches in our study. Their argumentation relied on two major points: (1) an incorrect assignment of vision system to four out of 22 sampled species in our study; and (2) the use of an incorrect approach for phylogenetic correction of the predicted associations. Here, we discuss in detail re‐assignation of vision systems in that study and propose alternative interpretation for current knowledge on spectrophotometric data of avian pigments. We reanalysed the data by using phylogenetic generalized least squares analyses that account for the alluded limitations of phylogenetically independent contrasts and, in accordance with the hypothesis, confirmed a significant influence of parental visual system on gape coloration. Our results proved to be robust to the assumptions on visual system evolution for Laniidae and nocturnal owls that Renoult et al. ( J. Evol. Biol., 2009 ) study suggested may have flawed our early findings. Thus, the hypothesis that selection has resulted in increased detectability of nestling by adjusting gape coloration to parental visual systems is currently supported by our comparative data.     

Evolution of female colours in birds: The role of female cost of reproduction and paternal care

Female ornamentation is frequently observed in animal species and is sometimes found as more evolutionary labile than male ornamentation. A complex array of factors may explain its presence and variation. Here we assessed the role of female cost of reproduction and paternal care. Both factors have been pinpointed as important by theoretical studies but have not been investigated yet in details at the interspecific level. We worked on 133 species of North temperate Passeriformes bird species for which both the clutch volume – here taken as the proxy of female cost of reproduction – and amount of paternal care are relatively well known. Using spectrometry, we measured the whole-body coloured plumage patches and quantified three metrics corresponding to brightness (i.e. achromatic component), colour chromaticity (i.e. intensity) and colour volume (i.e. diversity). We found a strong association between male and female colour metrics. Controlling for this association, we found additional small but detectable effects of both cost of reproduction and paternal care. First, females of species with more paternal care were slightly brighter. Second, the interaction between the level of paternal care and egg volume was correlated with female colour intensity: females with more paternal care were more chromatic, with this association mostly present when their investment in reproduction was low. Together these results suggest that female cost of reproduction and paternal care are part of the multiple factors explaining variation of female coloration, besides the strong covariation between male and female coloration.     

Persisting stemma neuropils in Chaoborus crystallinus (Diptera: Chaoboridae): Development and evolution of a bipartite visual system

Stemmata or “larval” eyes are of crucial importance for the understanding of the evolution and ontogeny of the hexapod's main visual organs, the compound eyes. Using classical neuroanatomical techniques, I showed that the persisting stemmata of Chaoborus imagos are connected to persisting stemma neuropils neighboring the first and second order neuropils of the compound eyes, and therefore also the imago possesses a stemma lamina and medulla closely associated with the architecture and the developmental pattern of those of the compound eyes. The findings are compared with other arthropods, e.g. accessory lateral eyes in Amandibulata and Myriapoda, suggesting some ancestral rather than derived character states. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

The evolution of jumping performance in anurans: morphological correlates and ecological implications

We investigated the evolution of anuran locomotor performance and its morphological correlates as a function of habitat use and lifestyles. We reanalysed a subset of the data reported by Zug (Smithson. Contrib. Zool. 1978; 276: 1–31) employing phylogenetically explicit statistical methods (n = 56 species), and assembled morphological data on the ratio between hind-limb length and snout-vent length (SVL) from the literature and museum specimens for a large subgroup of the species from the original paper (n = 43 species). Analyses using independent contrasts revealed that classifying anurans into terrestrial, semi-aquatic, and arboreal categories cannot distinguish between the effects of phylogeny and ecological diversification in anuran locomotor performance. However, a more refined classification subdividing terrestrial species into 'fossorials' and 'non-fossorials', and arboreal species into 'open canopy', 'low canopy' and 'high canopy', suggests that part of the variation in locomotor performance and in hind-limb morphology can be attributed to ecological diversification. In particular, fossorial species had significantly lower jumping performances and shorter hind limbs than other species after controlling for SVL, illustrating how the trade-off between burrowing efficiency and jumping performance has resulted in morphological specialization in this group.     

Differential correlates of diet and phylogeny on the shape of the premaxilla and anterior tooth in sparid fishes (Perciformes: Sparidae)

We explore the correlational patterns of diet and phylogeny on the shape of the premaxilla and anterior tooth in sparid fishes (Perciformes: Sparidae) from the western Mediterranean Sea. The premaxilla is less variable, and in spite of the presence of species-specific features, a common structural pattern is easily recognizable in all species (i.e. the ascending and the articular processes are fused in a single branch, as in many percoid fishes). In contrast, tooth shape is more variable, and different structural types can be recognized (e.g. canine-like or incisive). Coupling geometric morphometric and comparative methods we found that the relationship between shape, diet and phylogeny also differs between premaxilla and tooth. Thus, the shape of the premaxilla is significantly correlated with food type, whereas the shape of the teeth is not correlated with diet, and probably reflects the species phylogenetic relationships. Two biological roles, resistance against compressive forces generated in the buccal cavity and the size of the oral gape, would explain the ecomorphological patterns of the premaxilla. The premaxilla and anterior tooth appear to evolve at different rates (mosaic evolution) and represent an example of morphological traits belonging to the same functional unit but following uncoupled evolutionary pathways.     

中华蜜蜂视觉系统中神经胶质的组成和胚后发育

神经胶质作为视觉系统的重要成分之一, 对视觉系统的发育及功能起着重要的作用。本研究通过组织解剖观察、 免疫组织化学等技术, 对中华蜜蜂Apis cerana cerana幼虫和蛹的视觉系统中神经胶质的类型和发育过程进行了比较研究。研究表明： 在中华蜜蜂视觉系统中, 根据神经胶质的位置和形态主要分为表面神经胶质、 皮层神经胶质和神经纤维网神经胶质3种类型; 神经胶质主要来源于视柄和视叶中的神经胶质前体中心; 神经胶质细胞数量的增加一方面来自于细胞的迁移, 另一方面来自于神经胶质细胞自身的分裂增殖。本研究为昆虫神经胶质的发育以及功能研究提供理论基础。     

Miniaturization in plethodontid salamanders (Gaudata: Plethodontidae) and its consequences for the brain and visual system

In seven species of plethodontid salamanders (Desmognathus ochrophaeus, Eurycea bislineata, Plethodon cinereus, Batrachoseps attenuatus, Hydromantes italicus, Thorius narisovalis and Bolitoglossa subpalmata), absolute and relative volumes of the eye, the brain, major regions of the brain, and regions containing the major visual and visuomotor centres (i.e. thalamus, praetectum, tectum and tegmentum mesencephali), and the density and number of neurons in these regions were determined. The seven species range from moderately large to extremely small in body size and from the smallest to the largest genome sizes found in terrestrial salamanders. The following processes were observed in miniaturized salamanders with intermediate to large genome and cell sizes (Batrachoseps, Thorius) as compared to small and medium-sized salamanders with small genome and cell sizes: (1) increase in the relative size of the brain, from 3.9 to 12.4% of head volume; (2) reduction in relative size of the ventricles from 10.9 to 5.8% of brain volume; (3) increase in relative volume of those brain regions containing the major visual and visuomotor centres from 29.2 to 37% of brain volume; (4) increase in volume of grey matter relative to white matter, from 33.2 to 44.4% of midbrain volume; (5) increase in volume of tectal relative to tegmental grey matter, from 54.8 to 76.8% of total midbrain volume; (6) increase in neuron packing density in the regions containing the visual centres, from 16 to 31.5%. Because of these compensatory processes, Thorius, the smallest species with a head 1/27 and a brain 1/9 the size of that of the largest one, Hydromantes, has 1/3 as many central visual neurons (58 000 vs. 187 000). Some of these processes found in miniaturized salamanders, such as increase in tectal cell density, also occur in large salamanders with very large genome and cell sizes, viz. in Bolitoglossa (25%) and Hydromantes (29%). Thus, increase in genome size and cell size seem to pose functional problems similar to miniaturization; both cases involve an increase in cell size relative to overall organismal structure.     

The evolution of thermal performance curves in semi-aquatic newts: Thermal specialists on land and thermal generalists in water?

The position and shape of thermal performance curves (TPCs, the functions relating temperature to physiological performance) for ecologically relevant functions will directly affect the fitness of ectotherms and therefore should be under strong selection. However, thermodynamic considerations predict that relationships between the different components of the TPC will confound its evolutionary optimization. For instance, the “jack-of-all-temperatures” hypothesis predicts a trade-off between the breadth of the TPC and the maximal performance capacity; the “warmer is better” hypothesis suggests that low thermal optima will come with low absolute performances. Semi-aquatic organisms face the additional challenge of having to adjust their TPCs to two environments that are likely to differ in mean temperature and thermal variability. In this paper, we examine how parameters of the TPCs for maximal running and swimming speed have co-evolved in the semi-aquatic newt genus Triturus. We consider evolutionary relationships between the width and the height of the TPCs, the optimal temperatures and maximal performance. Phylogenetic comparative analyses reveal that in Triturus, swimming and running differ substantially in the (co-)variation of TPC parameters. Whereas evolutionary changes in the TPC for swimming primarily concern the shape of the curve (generalist versus specialist), most interspecific variation in running speed TPCs involves shifts in overall performance across temperatures.     

Rapid adaptation to a novel light environment: The importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.)

Colonization of novel habitats is typically challenging to organisms. In the initial stage after colonization, approximation to fitness optima in the new environment can occur by selection acting on standing genetic variation, modification of developmental patterns or phenotypic plasticity. Midas cichlids have recently colonized crater Lake Apoyo from great Lake Nicaragua. The photic environment of crater Lake Apoyo is shifted towards shorter wavelengths compared to great Lake Nicaragua and Midas cichlids from both lakes differ in visual sensitivity. We investigated the contribution of ontogeny and phenotypic plasticity in shaping the visual system of Midas cichlids after colonizing this novel photic environment. To this end, we measured cone opsin expression both during development and after experimental exposure to different light treatments. Midas cichlids from both lakes undergo ontogenetic changes in cone opsin expression, but visual sensitivity is consistently shifted towards shorter wavelengths in crater lake fish, which leads to a paedomorphic retention of their visual phenotype. This shift might be mediated by lower levels of thyroid hormone in crater lake Midas cichlids (measured indirectly as dio2 and dio3 gene expression). Exposing fish to different light treatments revealed that cone opsin expression is phenotypically plastic in both species during early development, with short and long wavelength light slowing or accelerating ontogenetic changes, respectively. Notably, this plastic response was maintained into adulthood only in the derived crater lake Midas cichlids. We conclude that the rapid evolution of Midas cichlids’ visual system after colonizing crater Lake Apoyo was mediated by a shift in visual sensitivity during ontogeny and was further aided by phenotypic plasticity during development.