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Evolutionary Shift from Fighting to Foraging in Blind Cavefish Through Changes in the Serotonin Network

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Evolutionary Shift from Fighting to Foraging in Blind Cavefish Through Changes in the Serotonin Network View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Current Biology 23, 1–10, January 7, 2013 ª2013 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2012.10.044 Article Evolutionary Shift from Fighting to Foraging in Blind Cavefish through Changes in the Serotonin Network Yannick Elipot,1 He´le`ne Hinaux,1 Jacques Callebert,2 accumulation of morphologically reducing, selectively neutral and Sylvie Re´taux1,* mutations [4]. More recently, emphasis was given to the impor- 1Equipe De´ veloppement Evolution du Cerveau Ante´ rieur, tance of selection on constructive traits and indirect effects on UPR3294 Neurobiologie et De´ veloppement, CNRS, Institut regressive traits, through mutations in pleiotropic develop- Alfred Fessard, 91198 Gif-sur-Yvette, France mental genes [5]. ‘‘Evo-devo’’ studies bring some support to 2Service Biochimie et Biologie Mole´ culaire, Hoˆ pital the latter scenario. Actually, in addition to the loss of their Lariboisie` re, 75475 Paris, France eyes, cavefish have larger olfactory bulbs and hypothalamus [6], more taste buds, more teeth, larger jaws [7], and more neu- romasts [8, 9]. Many of these anatomofunctional changes are Summary due to embryonic modifications in morphogen signaling, namely Sonic Hedgehog (Shh) and Fibroblast Growth Factor Background: Within the species Astyanax mexicanus, there (Fgf8) [10, 11]. These early signaling changes are indirectly are several interfertile populations of river-dwelling sighted responsible for lens apoptosis and thus eye degeneration fish and cave-dwelling blind fish which have evolved morpho- [11], but they also induce the development of an enhanced logical and behavioral adaptations, the origins of which are gustatory apparatus [7], of larger olfactory epithelium and unknown. Here, we have investigated the neural, genetic, olfactory bulbs, and of a larger hypothalamus [6, 10]. It is likely, and developmental bases for the evolution of aggressive even though it is not yet demonstrated, that these changes in behavior in this teleost. sensory and neuroendocrine systems are adaptive. Results: We used an intruder-resident behavioral assay to Cavefish and surface fish behavior is also very different, with compare aggressiveness quantitatively (attack counts) and important modifications concerning feeding and social qualitatively (pattern and nature of attacks) between the behavior. Cavefish are bottom feeders and explore the sub- surface and cave populations of Astyanax. Using this para- strate at a precise 45 angle [4]; they evolved a ‘‘vibration- digm, we characterize aggressive behavior in surface fish, attraction behavior’’ to locate food dropping onto the water bring support for the genetic component of this trait, and surface [9]; they display modified swimming kinematics and show that it is controlled by raphe serotonergic neurons and a ‘‘wall-following’’ behavior to avoid collisions and explore that it corresponds to the establishment of dominance their environment [12–14]; they have lost sleep, supposedly between fish. Cavefish have completely lost such aggres- to increase wakefulness and chances to find food [15]; cave- sive/dominance behavior. The few attacks performed by fish do well, in food competition experiments in the dark, cavefish during the behavioral test instead correspond to whereas surface fish starve [16]; and cavefish have lost the food-seeking behavior, driven by the developmental evolution aggressive behavior that is a trademark of their surface-fish of their hypothalamic serotonergic paraventricular neurons, counterparts [17–19]. These many and subtle behavioral adap- itself due to increased Sonic Hedgehog signaling during early tations are likely responsible for cavefish survival and success forebrain embryogenesis. during cave colonization. They represent complex traits, due Conclusions: We propose that during evolution and adapta- to many and subtle changes in specific brain regions. tion to their cave habitat, cavefish have undergone a behavioral We focused on the loss of aggressiveness in cavefish. We shift, due to modifications of their serotonergic neuronal characterized aggressive behavior in the two Astyanax network. They have lost the typical aggressive behavior of morphs, assessed its genetic basis, demonstrated the role of surface fish and evolved a food-seeking behavior that is prob- serotonin in the process, and investigated the developmental ably more advantageous to surviving in the dark. We have origin of the modifications in serotonergic network and therefore demonstrated a link between the development of behavior in cavefish. a neuronal network and the likely adaptive behaviors it controls. Results Introduction To compare aggressiveness in sighted surface fish (SF) and blind cavefish (CF) the classic ‘‘mirror test’’ is inappropriate. The Mexican tetra Astyanax mexicanus exists under two We used an ‘‘intruder assay’’ (see Figure S1A available online). morphs: sighted river morphs inhabiting the streams of Two fishes were habituated overnight in separate 200 ml Mexico, and 29 populations of blind and depigmented cave- tanks. The next morning, one fish was transferred into the fish morphs living in caves of the Sierra del Abra region, tank of the other, and their behavior was immediately recorded Mexico. Being from the same species and having diverged for 1 hr. about one million years ago, these fish constitute an outstanding model for evolutionary biology [1, 2]. Surface Fish and Cavefish Show Quantitative and At first the cavefish eyes were thought to degenerate Qualitative Differences in Aggressive Behavior because they were useless in caves [3]. Then, it was proposed SF were ten times more aggressive than Pacho´ n CF in the that eye and pigment loss was almost entirely the result of the intruder assay (Figure 1A and Movies S1 and S2). During 1 hr, two SF attacked each other more than 1,000 times (1,132 6 103; n = 57), whereas two Pacho´ n CF attacked each *Correspondence: [email protected] other about 100 times (110 6 11; n = 56). This quantitative Current Biology Vol 23 No 1 2 difference was accompanied by a qualitative difference in the pattern of attacks (Figures 1B and 1C). SF performed few attacks in the first 15 min, then became more aggressive and attacked with high frequency in the second half of the test (Figure 1B). Conversely, CF performed some attacks in the first 15–20 min and then swam quietly (Figure 1C). In order to assess the statistical significance of this difference in the pattern of attacks as a function of time, we used normalized cumulative curves and calculated the slopes of the tangents to these curves at three time points (10, 30, and 60 min; Figures 1D and S1B). The slopes of tangents therefore represent the frequency of attacks at a given moment of the test. The polynomial curves exhibited by SF resulted in a typical and significant ‘‘up’’ pattern for the slopes of tangents at the three time points (Figures 1D and 1E, blue), whereas the logarithmic curves exhibited by CF resulted in a typical and significant ‘‘down’’ pattern (Figures 1D and 1E, red). At the three time points examined, the slope values were different between SF and CF, showing that the pattern difference between the two Astyanax morphs is statistically significant. These results demonstrate that CF have lost most of the aggressive behavior that is a hallmark of their SF counterparts and that the ‘‘intruder assay’’ allows the detection of quantitative and qualitative behavioral differences. Attacks in SF Are Not Visually Driven, but Are Facilitated by Vision We next tested whether the lack of aggressive behavior in CF is due to their lack of vision. First, we blinded SF early in development by bilateral removal of their eye lenses at 40 hpf (hours postfertilization). Such early surgical lens ablation mimics the CF condition, in which the apoptotic lens induces eye degeneration [18, 20, 21]. Lens-ablated SF presented degenerated eyes at 3 months (Figures 2A and 2B), and their optic tectum contralateral to the ablated eye was hypomorphic (Figure 2C) (see also [22]). Their visual sense was absent when tested in a fear-predator test (Movie S3). Blind, bilaterally lens-ablated SF performed fewer attacks than siblings that were not operated on (Fig- ure 2D, green), but they still attacked significantly more than CF. Their pattern was ‘‘up’’ and indistinguishable from sighted SF controls (Figure 2E). Second, the resident-intruder assays were conducted in the dark, using infrared recordings. In these conditions, SF (and CF) behaved exactly alike in the light, both in terms of attack counts and attack patterns (Figures 2D and 2E, dark blue/ red). These data suggest that there is no requirement for vision in the expression of the SF aggressive behavior. Loss of Aggressive Behavior in Independently Evolved Cavefish Populations Parallel phenotypic diversification in closely related animals is a rigorous framework for testing the role of natural selection in (D) Normalized cumulative attack counts expressed as a percentage of total attacks and as a function of time in SF (blue) and in CF (red). (E) Slopes of the tangents of the cumulative curves in (D), respectively, taken Figure 1. Characterization of Aggressive Behavior in Surface Fish and Its at three time points during the test: 10, 30, and 60 min, in SF (blue, n = 57) Loss in Blind Cavefish and in CF (red, n = 56). For a detailed and complete description of the (A) Number of attacks counted during 1 hr between two surface fish method used, see Figure S1. Asterisks indicate p < 0.0001 (Mann-Whitney) (SF, blue) or between two blind cavefish (CF, red). In this and following when comparing corresponding values in SF and CF. figures, the n given in colored bars indicates the number of tests performed In this and the following figures, asterisks indicate significant differences in (hence the number of animals tested is 2 n). attack counts (Mann-Whitney). The pattern indicated (‘‘down,’’ ‘‘up,’’ or (B and C) Typical ODRec graphs showing the distribution of attacks as ‘‘flat’’) for each condition was statistically tested (Kruskal-Wallis and a function of time along the 1 hr test in a SF (B, blue) and in a CF (C, red).
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