Variation in Brain Anatomy in Frogs and Its Possible Bearing on Their Locomotor Ecology Adriana S
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Journal of Anatomy J. Anat. (2017) doi: 10.1111/joa.12613 Variation in brain anatomy in frogs and its possible bearing on their locomotor ecology Adriana S. Manzano,1 Anthony Herrel,2 Anne-Claire Fabre2 and Virginia Abdala3 1CONICET-UADER, Entre Rıos, Argentina 2Departement d’Ecologie et de Gestion de la Biodiversite, UMR 7179 C.N.R.S/M.N.H.N., Paris Cedex, France 3Facultad de Ciencias Naturales e Instituto Miguel Lillo, UNT-Horco Molle, Instituto de Biologıa Neotropical-CONICET, Tucuman, Argentina Abstract Despite the long-standing interest in the evolution of the brain, relatively little is known about variation in brain anatomy in frogs. Yet, frogs are ecologically diverse and, as such, variation in brain anatomy linked to differences in lifestyle or locomotor behavior can be expected. Here we present a comparative morphological study focusing on the macro- and micro-anatomy of the six regions of the brain and its choroid plexus: the olfactory bulbs, the telencephalon, the diencephalon, the mesencephalon, the rhombencephalon, and the cerebellum. We also report on the comparative anatomy of the plexus brachialis responsible for the innervation of the forelimbs. It is commonly thought that amphibians have a simplified brain organization, associated with their supposedly limited behavioral complexity and reduced motor skills. We compare frogs with different ecologies that also use their limbs in different contexts and for other functions. Our results show that brain morphology is more complex and more variable than typically assumed. Moreover, variation in brain morphology among species appears related to locomotor behavior as suggested by our quantitative analyses. Thus we propose that brain morphology may be related to the locomotor mode, at least in the frogs included in our analysis. Key words: anurans; central nervous system morphology; locomotion. Introduction allowing them to survive in a terrestrial environment. The central nervous system of anurans undergoes intrinsic The general organization and structure of the motor con- changes such as the development of an acoustic vocal sys- trol system is thought to be evolutionarily conserved among tem, a binocular visual system, and specializations for tetra- vertebrates. Indeed, the general ‘bauplan’ of the vertebrate pod limb movement. These critical changes are reflected in nervous system is similar from the forebrain to the spinal the anatomy of the brain and spinal cord. cord across many taxa (Grillner et al. 2007). Five vesicles Almost no variation in the gross anatomy of the brain has develop in the areas corresponding to the telencephalon, been reported in anurans. However, most of the studies the diencephalon, the mesencephalon, and the rhomben- have focused on ranid frogs, some species of toads, and cephalon in early embryos, in addition to the cerebellum Xenopus laevis, as summarized in the works of Gaupp and the brain stem. The transition from fish to amphibians (1896), Llinas & Precht (1976), and Ten Donkelaar (1998). marks the beginning of the origin of tetrapods and the Moreover, studies on the functional morphology of the cen- major adaptive radiation in vertebrate evolution. This went tral nervous system in frogs have focused mainly on the hand in hand with striking changes in brain morphology prey-capture visual system (Lettvin et al. 1968; Ewert, 1976, (Northcutt & Royce, 1975; Ten Donkelaar, 1998). Several fea- 1987; Borchers et al. 1978; Grobstein et al. 1983; Nishikawa tures characterize the first vertebrate group to pass from an et al. 1992; Gray & Nishikawa, 1995; Deban et al. 2001), and aquatic to a terrestrial mode of life. Most amphibians, and the vocalization and auditory systems (Edwards & Kelley, particularly anurans, are characterized by a larval period 2001). There are some experimental studies that suggest and a metamorphosis that changes many of the body parts, that in urodeles (salamanders) the brain does not differ in its anatomical or functional properties from that of anurans (Wicht & Himstedt, 1988). In contrast, a comparative Correspondence Adriana Manzano, CONICET-UADER, Matteri y Espana~ 3105, Entre anatomical study made by Taylor et al. (1995) in which the Rıos, Argentina. E: [email protected] brain of frogs with four different modes of life was ana- Accepted for publication 8 March 2017 lyzed, proposed that a relationship between ecological © 2017 Anatomical Society 2 Variation in brain anatomy in frogs, A. Manzano et al. habits and brain morphology exists. Taylor et al. (1995) substances over their body, a behavior called ‘wiping’ by specifically tested whether the six brain regions (the main Blaylock et al. (1976). Also frogs use complex forelimb olfactory bulbs, the accessory olfactory bulbs, the telen- movements when building ‘leaf nests’ to deposit eggs (Lilly- cephalon, the optic tectum, the cerebellum, and the brain white et al. 1998). Finally, Manzano et al. (2008) and Herrel stem) were different in terrestrial, arboreal, fossorial, and et al. (2013) observed differences in the use of the hand to aquatic frogs. Their results indicated that despite the overall grasp narrow substrates during locomotion in arboreal similarity of anuran brains, some interesting differences and frogs. apparent adaptations to fossorial and arboreal modes of life Based on the presence of skilled limb movement in arbo- do appear to exist. This is in accordance with the results of a real frogs we hypothesize that the central nervous system recent study evaluating the effects of phylogeny and ecol- may show variation in gross anatomy in taxa capable of ogy on the evolution of brain size in frogs (Liao et al. 2015). these movements. We here provide a comparative morpho- These authors concluded that whereas ecology did not logical study focusing on the macro- and micro-anatomy of impact overall brain size, habitat and diet type did impact the six regions of the brain and its choroid plexus: the olfac- the size of the telencephalon (Liao et al. 2015). tory bulbs, the telencephalon, the diencephalon, the mes- Yet, anurans are capable of engaging in different com- encephalon, the rhombencephalon, and the cerebellum. plex behaviors independent of their mode of life, often We compare frogs with different ecologies that accordingly reflected in the use of the hands and feet. Indeed, frogs use their limbs in different contexts, specifically focusing on can perform skilled movements using their wrists and the difference between arboreal frogs and those with other hands (Gray et al. 1997; Manzano et al. 2008; Sustaita et al. locomotor modes. We also report on the comparative anat- 2013). Limb movement implies complex interactions of the omy of the plexus brachialis responsible for the innervation sensory and central nervous systems, muscular mechanics, of the forelimbs. Our main objectives were thus to investi- and the interaction with the environment. Iwaniuk & gate: (i) the diversity in brain morphology across a range of Whishaw (2000) stressed that skilled forelimb movements frogs exhibiting different locomotor modes, and (ii) provide are common among tetrapod taxa and probably share a a preliminary analysis of the relationship between morphol- common origin. They considered that skilled movements of ogy and locomotor mode. the limbs are homologous among tetrapods and likely derived from an elaborated food-handling behavior; how- Methods ever, this remains to be tested. The use of the hands in anu- rans has been studied, focusing on the diverse types of Gross anatomy movements possible. For example, skilled wrist movements have been shown to be present in arboreal frogs using The brain and spinal cord of formalin-fixed specimens of adult frogs of three suprageneric taxa proposed by Frost et al. (2006) and their hands to reach and grab prey and pushing it into, or Duellman et al. (2016) were dissected. They belong to Microhylidae: pulling it out of, the mouth (Gray et al. 1997). Moreover, Elachistocleis bicolor (n = 4 – Gastrophryninae); Phyllomedusidae: some frogs can perform other kinds of complex movements Phyllomedusa sauvagii (n = 3), Phyllomedusa hypochondrialis using their hands, for example when spreading lipid (n = 1), Phyllomedusa boliviana (n = 2); Hylidae: Pseudis minuta Table 1 Summary of measurements of the different brain areas. Olfactory bulbs Telencephalon Diencephalon Sp Lm Height Width Length Height Width Length Height Width Length Eb TB 0.43 Æ 0.04 0.85 Æ 0.13 0.44 Æ 0.1 0.56 Æ 0.07 1.53 Æ 0.18 1.01 Æ 0.18 0.57 Æ 0.04 0.61 Æ 0.11 0.40 Æ 0.05 Hp AJ 0.37 Æ 0.08 0.72 Æ 0.10 0.32 Æ 0.03 0.92 Æ 0.05 1.40 Æ 0.06 1.60 Æ 0.14 0.85 Æ 0.04 1.14 Æ 0.04 0.67 Æ 0.06 Ll TJ 0.39 Æ 0.02 0.62 Æ 0.02 0.38 Æ 0.04 0.80 Æ 0.09 0.85 Æ 0.03 1.36 Æ 0.14 0.75 Æ 0.16 0.71 Æ 0.06 0.69 Æ 0.02 Pb AW 0.56 0.43 1.09 0.87 1.92 1.89 0.66 1.26 0.77 Ph AW 0.41 0.71 0.36 0.81 1.15 1.15 0.73 0.75 0.68 Pm SW 0.50 Æ 0.08 0.60 Æ 0.10 0.44 Æ 0.03 1.03 Æ 0.11 1.28 Æ 0.20 1.56 Æ 0.02 0.84 Æ 0.10 1.04 Æ 0.14 0.51 Æ 0.06 Ps AW 0.70 Æ 0.19 1.38 Æ 0.37 0.44 Æ 0.02 1.34 Æ 0.30 1.92 Æ 0.12 1.66 Æ 0.05 1.23 Æ 0.09 1.28 Æ 0.22 0.80 Æ 0.15 Rf TH 0.50 Æ 0.13 0.83 Æ 0.08 0.27 Æ 0.07 0.98 Æ 0.15 1.69 Æ 0.23 1.36 Æ 0.12 0.81 Æ 0.07 0.91 Æ 0.19 0.53 Æ 0.05 Sf AJ 0.70 Æ 0.11 0.84 Æ 0.11 0.24 Æ 0.06 1.06 Æ 0.07 1.38 Æ 0.26 1.75 Æ 0.10 1.03 Æ 0.04 1.06 Æ 0.08 0.64 Æ 0.14 Table entries are means (in mm) Æ standard deviations.