Current Biology Vol 24 No 11 R520
6.
7.
8.
9.
10.
11.
anaerobic parasitic protozoa. Biochimie 100, 3–17. Mu¨ller, M., Mentel, M., van Hellemond, J.J., Henze, K., Woehle, C., Gould, S.B., Yu, R.Y., van der Giezen, M., Tielens, A.G., and Martin, W.F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444–495. Shiflett, A., and Johnson, P.J. (2010). Mitochondrion-related organelles in parasitic eukaryotes. Annu. Rev. Microbiol. 64, 409–429. Brown, M.W., Sharpe, S.C., Silberman, J.D., Heiss, A.A., Lang, B.F., Simpson, A.G., and Roger, A.J. (2013). Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc. Biol. Sci. 280, 20131755. Gill, E.E., Diaz-Trivin˜o, S., Barbera`, M.J., Silberman, J.D., Stechmann, A., Gaston, D., Tamas, I., and Roger, A.J. (2007). Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Mol. Microbiol. 66, 1306–1320. Mus, F., Dubini, A., Seibert, M., Posewitz, M.C., and Grossman, A.R. (2007). Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathwys. J. Biol. Chem. 282, 25475–25486. Chaudhuri, M., Ott, R.D., and Hill, G.C. (2006). Trypanosome alternative oxidase: from
12.
13.
14.
15.
16.
17.
molecule to function. Trends Parasitol. 22, 481–491. Martin, W., and Muller, M. (1998). The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41. Michae¨l, D.K., Simone, D., Emmanuel, C., Guy, M., Fabienne, T., Ge´rard, P., Vale´rie, B., Eric, P., Philippe, B., Patrick, W., et al. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450–453. Burri, L., Williams, B.A.P., Bursac, D., Lithgow, T., and Keeling, P.J. (2006). Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc. Natl. Acad. Sci. USA 103, 15916–15920. Maralikova, B., Ali, V., Nakada-Tsukui, K., Nozaki, T., Van Der Giezen, M., Henze, K., and Tovar, J. (2010). Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria. Cell. Microbiol. 12, 331–342. Ny´vltova´a, E., Suta´k, R., Harantb, K., Sedinova´, M., Hrdy´a, I., Paces, J., Cestmı´r, V., and Tachezy, J. (2013). NIF-type iron-sulfur cluster assembly system is duplicated and distributed in the mitochondria and cytosol of Mastigamoeba balamuthi. Proc. Natl. Acad. Sci. USA 110, 7371–7376. van der Giezen, M., Cox, S., and Tovar, J. (2004). The iron-sulfur cluster assembly genes iscS and iscU of Entamoeba histolytica were
Neuroethology: Self-Recognition Helps Octopuses Avoid Entanglement How an octopus performs complex movements of its eight sucker-studded arms without entanglement has been a mystery. A new study has found that self-recognition of the octopus’s skin by its suckers inhibits reflexive grasping of its own arms, simplifying the mechanisms needed to generate intricate arm behavior. Robyn J. Crook and Edgar T. Walters* A couple learning to dance soon realizes how easy it is for eight active limbs to become entangled. The challenge to an octopus is far greater because each of its eight supple arms can bend in almost any direction from any point along its boneless length. Worse, the arms have numerous suckers that reflexively grasp whatever they touch. But with a few hundred million years more time than that available to human dancers to solve the limb entanglement problem, the octopus has evolved a solution based on a mechanism more familiar to immunologists than to neurobiologists: chemical self-recognition. In a study reported in this issue of Current Biology, Nesher et al. [1] demonstrate that a cue in the skin of octopus inhibits sucker attachment, helping to avoid inadvertent grasping of its own arms as
each arm performs its graceful routines. Unlike human couples who struggle to synchronize movements commanded by just two brains, an octopus effectively has nine brains that have their own agendas: each of its eight arms has a large and relatively complete nervous system, which seems barely to communicate with the other arms [2,3]. The central brain sends general executive commands to all the arms at once, but these messages lack detailed instructions, leaving the individual arms remarkable autonomy to control their own movements [4,5]. Central encoding of arm position appears to be lacking; for example, somatotopically arranged sensory and motor representations of the octopus body within its brain are absent [6]. And while octopuses can learn to use visual feedback to guide an arm to a specific location [7], visual control of more than one arm at a time
acquired by horizontal gene transfer. BMC Evol. Biol. 4, 7. 18. Goldberg, A.V., Molik, S., Tsaousis, A.D., Neumann, K., Kuhnke, G., Delbac, F., Vivares, C.P., Hirt, R.P., Lill, R., and Embley, T.M. (2008). Localization and functionality of microsporidian iron–sulphur cluster assembly proteins. Nature 452, 624–648. 19. Lill, R., and Kispal, G. (2000). Maturation of cellular Fe–S proteins: an essential function of mitochondria. Trends Biochem. Sci. 25, 352–356. 20. Hampl, V., Stairs, C.W., and Roger, A.J. (2011). The tangled past of eukaryotic enzymes involved in anaerobic metabolism. Mob. Genet. Elements 1, 71–74. 1Department
of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. 2Department of Genetics, Evolution and Ecology, University College London, Gower Street, London, WC1E 6BT, UK. 3Biosciences, University of Exeter, Geoffrey Pope Building, Exeter, EX4 4QD, UK. *E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2014.03.075
is not apparent. So, without the brain or eyes telling each arm where it is and where the seven others are, some sort of local sensing and control are needed. In a series of systematic experiments using the common octopus (Octopus vulgaris), Nesher et al. [1] first showed that the suckers of amputated octopus arms recognize skin from the same species. Suckers attached avidly to abiotic surfaces and to potential food items, but the suckers of amputated arms neither grasped skin of their own arm nor of other arms from the same octopus or other octopuses. Strong evidence for species recognition by individual suckers came from offering to amputated arms a petri dish containing a semi-circular slice of isolated skin covering half the glass: the suckers attached firmly to the glass, but adjacent suckers touching the skin refused to attach. What is the cue that tells an octopus sucker to avoid skin from its own species? Avoidance did not occur when the researchers presented amputated arms with skinned pieces of octopus arm, indicating that cues for species recognition are in the skin. Presentation of various skin extracts suggested that the cue molecules are hydrophobic, but their identity remains a mystery. The new findings of Nesher et al. [1] are the first evidence for the use of a
Dispatch R521
chemical recognition cue for motor control: yet another surprising way that this brainiest of all invertebrates generates complex arm behavior. The nervous system of the octopus arm has been an object of intense study for more that 60 years [3,8]. Each sucker is controlled by its own small ganglion, which contains the cell bodies of primary mechanosensory and chemosensory neurons that innervate the rim of the sucker [9]. The individual suckers are networked together, so that coordinated movements involved in advancing the arm along a surface or passing food items from one sucker to the next toward the mouth are controlled by local networks of sucker ganglia and larger axial ganglia spaced regularly along the main arm nerve cord [10]. Evidence from isolated arms and decerebrated octopuses indicates that the release of suction is commanded by the central brain; in its absence, the suckers adhere tightly and seemingly lose their ability to release once attached [11]. Nesher et al. [1] show that the central brain can override this local inhibition of suction when the animal wants something to eat. This explains how octopuses engage in cannibalism and, occasionally, also in autophagy — eating part of their own body [12]. Octopuses eat by grasping food with their arms, using their suckers to convey the food mouthward. This also occurs in amputated arms, with the suckers passing food items proximally despite the absence of central neural control. Release of the local inhibitory effects of chemical recognition of octopus skin by the suckers is clearly necessary for cannibalism and autophagy. Nesher et al.’s [1] studies of the executive role of the central brain in releasing local inhibition of sucker reflexes revealed another surprise: contact chemical cues let an octopus distinguish its own skin from that of conspecifics. Intact octopuses offered their own (self) and non-self amputated arms found the non-self arms more appetizing and easier to handle. Self arms were less likely to be consumed than arms from other octopuses and, when an octopus did attempt to consume its own amputated arm, the arm was held solely (and awkwardly) by the octopus’s beak while it was eaten. This suggests that considerable central brain effort is involved in overriding local sucker control; as soon as an
amputated self arm is grasped by the mouth, all of the suckers release their hold on the amputated arm. In contrast, amputated non-self arms tend to be held like any other food item throughout the meal, being grasped by suckers on the remaining arms until the amputated arm is consumed. Chemical self-recognition mechanisms are of course nothing new — from cellular to organismal levels, being able to distinguish self from non-self is vitally important. For example, chemical cues permit the simplest animals, sponges, to distinguish between their own and foreign tissues, and studies of this process have provided a great deal of information about the evolution of innate immunity [13–15]. Selfrecognition is an essential tool of the immune system, helping animals and plants ward off infectious agents [16], reject foreign bodies, and defend against the body’s own cells gone bad in cancer [17]. Similar recognition mechanisms minimize entanglement of a neuron’s own branches by avoiding self contact within dendritic arbors [18]. An interesting parallel to the entanglement problem of octopus arms is found in sea anenomes, corals, and other cnidarians, which also have a profusion of flexible appendages — tentacles — equipped with stinging nematocysts that also are reflexively activated by contact with living tissue. Cnidarians utilize chemical cues to avoid discharging their nematocysts onto themselves [19], while deploying them to ward off territorial threats from competing cnidarian species, including different clones of the same species [20]. The unexpected operation of self-recognition mechanisms in the moment-to-moment control of elaborate motor patterns in octopuses raises interesting questions about whether the complex nervous system of this animal has access to chemosensory information about contact of its arms with its skin. For example, when an octopus touches its own amputated arm and chooses to eat it, is the central brain ‘‘aware’’ in any sense that its intended meal is its own tissue? This fascinating report [1] has disclosed a new use for chemical self-recognition. Added to the octopus’s distinctive and very complicated neural control networks, an apparently simple chemosensory
mechanism for discriminating between self and non-self enables intricate dances of eight highly independent limbs, allowing them to move together fluidly and effectively. References 1. Nesher, N., Levy, G., Grasso, F.W., and Hochner, B. (2014). Self-recognition mechanism between skin and suckers prevents octopus arms from interfering with each other. Curr. Biol. 24, 1271–1275. 2. Budelmann, B., and Young, J. (1985). Central pathways of the nerves of the arms and mantle of Octopus. Philos. Trans. R. Soc. Lond. B 310, 109–122. 3. Rowell, C. (1963). Excitatory and inhibitory pathways in the arm of Octopus. J. Exp. Biol. 40, 257–270. 4. Sumbre, G., Gutfreund, Y., Fiorito, G., Flash, T., and Hochner, B. (2001). Control of Octopus arm extension by a peripheral motor program. Science 5536, 1845–1848. 5. Gutfreund, Y., Matzner, H., Flash, T., and Hochner, B. (2006). Patterns of motor activity in the isolated nerve cord of the octopus arm. Biol. Bull. 211, 212–222. 6. Zullo, L., Sumbre, G., Agnisola, C., Flash, T., and Hochner, B. (2009). Nonsomatotopic organization of the higher motor centers in octopus. Curr. Biol. 19, 1632–1636. 7. Gutnick, T., Byrne, R.A., Hochner, B., and Kuba, M. (2011). Octopus vulgaris uses visual information to determine the location of its arm. Curr. Biol. 21, 460–462. 8. Altman, J. (1971). Control of accept and reject reflexes in the Octopus. Nature 229, 204–206. 9. Graziadei, P. (1962). Receptors in the suckers of Octopus. Nature 195, 57–59. 10. Grasso, F.W. (2008). Octopus sucker-arm coordination in grasping and manipulation. Am. Malacol. Bull. 24, 13–23. 11. Rowell, C.H.F. (1966). Activity of interneurones in the arm of Octopus in response to tactile stimulation. J. Exp. Biol. 44, 589–605. 12. Budelmann, B.U. (1998). Autophagy in Octopus. South African J. Mar. Sci. 20, 101–108. 13. Amano, S. (1990). Self and non-self recognition in a calcareous sponge, Leucandra abratsbo. Biol. Bull. 179, 272–278. 14. Stoddart, J., and Ayre, D. (1985). Selfrecognition in sponges and corals? Evolution (NY) 39, 461–463. 15. Dishaw, L.J., and Litman, G.W. (2009). Invertebrate allorecognition: the origins of histocompatibility. Curr. Biol. 19, R286–R288. 16. Medzhitov, R., and Janeway, C. (2002). Decoding the patterns of self and nonself by the innate immune system. Science 296, 298–300. 17. Houghton, A. (1994). Cancer antigens: immune recognition of self and altered self. J. Exp. Med. 180, 1–4. 18. Zipursky, S.L., and Sanes, J.R. (2010). Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143, 343–353. 19. Ertman, S., and Davenport, D. (1981). Tentacular nematocyte discharge and self-recognition in Anthopleura elegantissima Brandt. Biol. Bull. 161, 366–370. 20. Hidaka, M., Yurugi, K., Sunagawa, S., and Kinzie, R.K. (1997). Contact reactions between young colonies of the coral Pocillopora damicornis. Coral Reefs 16, 13–20.
Department of Integrative Biology and Pharmacology University of Texas Medical School at Houston, 6431 Fannin St, Houston, TX 77030 USA. *E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2014.04.036
6.
7.
8.
9.
10.
11.
anaerobic parasitic protozoa. Biochimie 100, 3–17. Mu¨ller, M., Mentel, M., van Hellemond, J.J., Henze, K., Woehle, C., Gould, S.B., Yu, R.Y., van der Giezen, M., Tielens, A.G., and Martin, W.F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444–495. Shiflett, A., and Johnson, P.J. (2010). Mitochondrion-related organelles in parasitic eukaryotes. Annu. Rev. Microbiol. 64, 409–429. Brown, M.W., Sharpe, S.C., Silberman, J.D., Heiss, A.A., Lang, B.F., Simpson, A.G., and Roger, A.J. (2013). Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc. Biol. Sci. 280, 20131755. Gill, E.E., Diaz-Trivin˜o, S., Barbera`, M.J., Silberman, J.D., Stechmann, A., Gaston, D., Tamas, I., and Roger, A.J. (2007). Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Mol. Microbiol. 66, 1306–1320. Mus, F., Dubini, A., Seibert, M., Posewitz, M.C., and Grossman, A.R. (2007). Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathwys. J. Biol. Chem. 282, 25475–25486. Chaudhuri, M., Ott, R.D., and Hill, G.C. (2006). Trypanosome alternative oxidase: from
12.
13.
14.
15.
16.
17.
molecule to function. Trends Parasitol. 22, 481–491. Martin, W., and Muller, M. (1998). The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41. Michae¨l, D.K., Simone, D., Emmanuel, C., Guy, M., Fabienne, T., Ge´rard, P., Vale´rie, B., Eric, P., Philippe, B., Patrick, W., et al. (2001). Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450–453. Burri, L., Williams, B.A.P., Bursac, D., Lithgow, T., and Keeling, P.J. (2006). Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc. Natl. Acad. Sci. USA 103, 15916–15920. Maralikova, B., Ali, V., Nakada-Tsukui, K., Nozaki, T., Van Der Giezen, M., Henze, K., and Tovar, J. (2010). Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria. Cell. Microbiol. 12, 331–342. Ny´vltova´a, E., Suta´k, R., Harantb, K., Sedinova´, M., Hrdy´a, I., Paces, J., Cestmı´r, V., and Tachezy, J. (2013). NIF-type iron-sulfur cluster assembly system is duplicated and distributed in the mitochondria and cytosol of Mastigamoeba balamuthi. Proc. Natl. Acad. Sci. USA 110, 7371–7376. van der Giezen, M., Cox, S., and Tovar, J. (2004). The iron-sulfur cluster assembly genes iscS and iscU of Entamoeba histolytica were
Neuroethology: Self-Recognition Helps Octopuses Avoid Entanglement How an octopus performs complex movements of its eight sucker-studded arms without entanglement has been a mystery. A new study has found that self-recognition of the octopus’s skin by its suckers inhibits reflexive grasping of its own arms, simplifying the mechanisms needed to generate intricate arm behavior. Robyn J. Crook and Edgar T. Walters* A couple learning to dance soon realizes how easy it is for eight active limbs to become entangled. The challenge to an octopus is far greater because each of its eight supple arms can bend in almost any direction from any point along its boneless length. Worse, the arms have numerous suckers that reflexively grasp whatever they touch. But with a few hundred million years more time than that available to human dancers to solve the limb entanglement problem, the octopus has evolved a solution based on a mechanism more familiar to immunologists than to neurobiologists: chemical self-recognition. In a study reported in this issue of Current Biology, Nesher et al. [1] demonstrate that a cue in the skin of octopus inhibits sucker attachment, helping to avoid inadvertent grasping of its own arms as
each arm performs its graceful routines. Unlike human couples who struggle to synchronize movements commanded by just two brains, an octopus effectively has nine brains that have their own agendas: each of its eight arms has a large and relatively complete nervous system, which seems barely to communicate with the other arms [2,3]. The central brain sends general executive commands to all the arms at once, but these messages lack detailed instructions, leaving the individual arms remarkable autonomy to control their own movements [4,5]. Central encoding of arm position appears to be lacking; for example, somatotopically arranged sensory and motor representations of the octopus body within its brain are absent [6]. And while octopuses can learn to use visual feedback to guide an arm to a specific location [7], visual control of more than one arm at a time
acquired by horizontal gene transfer. BMC Evol. Biol. 4, 7. 18. Goldberg, A.V., Molik, S., Tsaousis, A.D., Neumann, K., Kuhnke, G., Delbac, F., Vivares, C.P., Hirt, R.P., Lill, R., and Embley, T.M. (2008). Localization and functionality of microsporidian iron–sulphur cluster assembly proteins. Nature 452, 624–648. 19. Lill, R., and Kispal, G. (2000). Maturation of cellular Fe–S proteins: an essential function of mitochondria. Trends Biochem. Sci. 25, 352–356. 20. Hampl, V., Stairs, C.W., and Roger, A.J. (2011). The tangled past of eukaryotic enzymes involved in anaerobic metabolism. Mob. Genet. Elements 1, 71–74. 1Department
of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK. 2Department of Genetics, Evolution and Ecology, University College London, Gower Street, London, WC1E 6BT, UK. 3Biosciences, University of Exeter, Geoffrey Pope Building, Exeter, EX4 4QD, UK. *E-mail: [email protected]
http://dx.doi.org/10.1016/j.cub.2014.03.075
is not apparent. So, without the brain or eyes telling each arm where it is and where the seven others are, some sort of local sensing and control are needed. In a series of systematic experiments using the common octopus (Octopus vulgaris), Nesher et al. [1] first showed that the suckers of amputated octopus arms recognize skin from the same species. Suckers attached avidly to abiotic surfaces and to potential food items, but the suckers of amputated arms neither grasped skin of their own arm nor of other arms from the same octopus or other octopuses. Strong evidence for species recognition by individual suckers came from offering to amputated arms a petri dish containing a semi-circular slice of isolated skin covering half the glass: the suckers attached firmly to the glass, but adjacent suckers touching the skin refused to attach. What is the cue that tells an octopus sucker to avoid skin from its own species? Avoidance did not occur when the researchers presented amputated arms with skinned pieces of octopus arm, indicating that cues for species recognition are in the skin. Presentation of various skin extracts suggested that the cue molecules are hydrophobic, but their identity remains a mystery. The new findings of Nesher et al. [1] are the first evidence for the use of a
Dispatch R521
chemical recognition cue for motor control: yet another surprising way that this brainiest of all invertebrates generates complex arm behavior. The nervous system of the octopus arm has been an object of intense study for more that 60 years [3,8]. Each sucker is controlled by its own small ganglion, which contains the cell bodies of primary mechanosensory and chemosensory neurons that innervate the rim of the sucker [9]. The individual suckers are networked together, so that coordinated movements involved in advancing the arm along a surface or passing food items from one sucker to the next toward the mouth are controlled by local networks of sucker ganglia and larger axial ganglia spaced regularly along the main arm nerve cord [10]. Evidence from isolated arms and decerebrated octopuses indicates that the release of suction is commanded by the central brain; in its absence, the suckers adhere tightly and seemingly lose their ability to release once attached [11]. Nesher et al. [1] show that the central brain can override this local inhibition of suction when the animal wants something to eat. This explains how octopuses engage in cannibalism and, occasionally, also in autophagy — eating part of their own body [12]. Octopuses eat by grasping food with their arms, using their suckers to convey the food mouthward. This also occurs in amputated arms, with the suckers passing food items proximally despite the absence of central neural control. Release of the local inhibitory effects of chemical recognition of octopus skin by the suckers is clearly necessary for cannibalism and autophagy. Nesher et al.’s [1] studies of the executive role of the central brain in releasing local inhibition of sucker reflexes revealed another surprise: contact chemical cues let an octopus distinguish its own skin from that of conspecifics. Intact octopuses offered their own (self) and non-self amputated arms found the non-self arms more appetizing and easier to handle. Self arms were less likely to be consumed than arms from other octopuses and, when an octopus did attempt to consume its own amputated arm, the arm was held solely (and awkwardly) by the octopus’s beak while it was eaten. This suggests that considerable central brain effort is involved in overriding local sucker control; as soon as an
amputated self arm is grasped by the mouth, all of the suckers release their hold on the amputated arm. In contrast, amputated non-self arms tend to be held like any other food item throughout the meal, being grasped by suckers on the remaining arms until the amputated arm is consumed. Chemical self-recognition mechanisms are of course nothing new — from cellular to organismal levels, being able to distinguish self from non-self is vitally important. For example, chemical cues permit the simplest animals, sponges, to distinguish between their own and foreign tissues, and studies of this process have provided a great deal of information about the evolution of innate immunity [13–15]. Selfrecognition is an essential tool of the immune system, helping animals and plants ward off infectious agents [16], reject foreign bodies, and defend against the body’s own cells gone bad in cancer [17]. Similar recognition mechanisms minimize entanglement of a neuron’s own branches by avoiding self contact within dendritic arbors [18]. An interesting parallel to the entanglement problem of octopus arms is found in sea anenomes, corals, and other cnidarians, which also have a profusion of flexible appendages — tentacles — equipped with stinging nematocysts that also are reflexively activated by contact with living tissue. Cnidarians utilize chemical cues to avoid discharging their nematocysts onto themselves [19], while deploying them to ward off territorial threats from competing cnidarian species, including different clones of the same species [20]. The unexpected operation of self-recognition mechanisms in the moment-to-moment control of elaborate motor patterns in octopuses raises interesting questions about whether the complex nervous system of this animal has access to chemosensory information about contact of its arms with its skin. For example, when an octopus touches its own amputated arm and chooses to eat it, is the central brain ‘‘aware’’ in any sense that its intended meal is its own tissue? This fascinating report [1] has disclosed a new use for chemical self-recognition. Added to the octopus’s distinctive and very complicated neural control networks, an apparently simple chemosensory
mechanism for discriminating between self and non-self enables intricate dances of eight highly independent limbs, allowing them to move together fluidly and effectively. References 1. Nesher, N., Levy, G., Grasso, F.W., and Hochner, B. (2014). Self-recognition mechanism between skin and suckers prevents octopus arms from interfering with each other. Curr. Biol. 24, 1271–1275. 2. Budelmann, B., and Young, J. (1985). Central pathways of the nerves of the arms and mantle of Octopus. Philos. Trans. R. Soc. Lond. B 310, 109–122. 3. Rowell, C. (1963). Excitatory and inhibitory pathways in the arm of Octopus. J. Exp. Biol. 40, 257–270. 4. Sumbre, G., Gutfreund, Y., Fiorito, G., Flash, T., and Hochner, B. (2001). Control of Octopus arm extension by a peripheral motor program. Science 5536, 1845–1848. 5. Gutfreund, Y., Matzner, H., Flash, T., and Hochner, B. (2006). Patterns of motor activity in the isolated nerve cord of the octopus arm. Biol. Bull. 211, 212–222. 6. Zullo, L., Sumbre, G., Agnisola, C., Flash, T., and Hochner, B. (2009). Nonsomatotopic organization of the higher motor centers in octopus. Curr. Biol. 19, 1632–1636. 7. Gutnick, T., Byrne, R.A., Hochner, B., and Kuba, M. (2011). Octopus vulgaris uses visual information to determine the location of its arm. Curr. Biol. 21, 460–462. 8. Altman, J. (1971). Control of accept and reject reflexes in the Octopus. Nature 229, 204–206. 9. Graziadei, P. (1962). Receptors in the suckers of Octopus. Nature 195, 57–59. 10. Grasso, F.W. (2008). Octopus sucker-arm coordination in grasping and manipulation. Am. Malacol. Bull. 24, 13–23. 11. Rowell, C.H.F. (1966). Activity of interneurones in the arm of Octopus in response to tactile stimulation. J. Exp. Biol. 44, 589–605. 12. Budelmann, B.U. (1998). Autophagy in Octopus. South African J. Mar. Sci. 20, 101–108. 13. Amano, S. (1990). Self and non-self recognition in a calcareous sponge, Leucandra abratsbo. Biol. Bull. 179, 272–278. 14. Stoddart, J., and Ayre, D. (1985). Selfrecognition in sponges and corals? Evolution (NY) 39, 461–463. 15. Dishaw, L.J., and Litman, G.W. (2009). Invertebrate allorecognition: the origins of histocompatibility. Curr. Biol. 19, R286–R288. 16. Medzhitov, R., and Janeway, C. (2002). Decoding the patterns of self and nonself by the innate immune system. Science 296, 298–300. 17. Houghton, A. (1994). Cancer antigens: immune recognition of self and altered self. J. Exp. Med. 180, 1–4. 18. Zipursky, S.L., and Sanes, J.R. (2010). Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143, 343–353. 19. Ertman, S., and Davenport, D. (1981). Tentacular nematocyte discharge and self-recognition in Anthopleura elegantissima Brandt. Biol. Bull. 161, 366–370. 20. Hidaka, M., Yurugi, K., Sunagawa, S., and Kinzie, R.K. (1997). Contact reactions between young colonies of the coral Pocillopora damicornis. Coral Reefs 16, 13–20.
Department of Integrative Biology and Pharmacology University of Texas Medical School at Houston, 6431 Fannin St, Houston, TX 77030 USA. *E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2014.04.036
