- Email: [email protected]
Camouflage: Being Invisible in the Open Ocean
Current Biology
Dispatches 4. Rutishauser, U., Mamelak, A.N., and Adolphs, R. (2015). The primate amygdala in social perception - insights from electrophysiological recordings and stimulation. Trends Neurosci. 38, 295–306. 5. Wang, S., Tudusciuc, O., Mamelak, A.N., Ross, I.B., Adolphs, R., and Rutishauser, U. (2014). Neurons in the human amygdala selective for perceived emotion. Proc. Natl. Acad. Sci. USA 111, E3110–E3119. 6. Grabenhorst, F., Hernadi, I., and Schultz, W. (2012). Prediction of economic choice by primate amygdala neurons. Proc. Natl. Acad. Sci. USA 109, 18950–18955. 7. Haber, S.N., and Knutson, B. (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26.
visual stimuli during learning. Nature 439, 865–870.
of future events. Phil. Trans. R. Soc. Lond. B 364, 1245–1253.
10. Jenison, R.L., Rangel, A., Oya, H., Kawasaki, H., and Howard, M.A. (2011). Value encoding in single neurons in the human amygdala during decision making. J. Neurosci. 31, 331–338.
16. Mosher, C.P., Zimmerman, P.E., and Gothard, K.M. (2014). Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Curr. Biol. 20, 2459–2464.
11. Kim, S., Hwang, J., and Lee, D. (2008). Prefrontal coding of temporally discounted values during intertemporal choice. Neuron 59, 161–172.
17. Chang, S.W., Fagan, N.A., Toda, K., Utevsky, A.V., Pearson, J.M., and Platt, M.L. (2015). Neural mechanisms of social decision-making in the primate amygdala. Proc. Natl. Acad. Sci. USA 112, 16012–16017.
12. Sescousse, G., Redoute, J., and Dreher, J.C. (2010). The architecture of reward value coding in the human orbitofrontal cortex. J. Neurosci. 30, 13095–13104. 13. Bush, G., Luu, P., and Posner, M.I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222.
8. Hampton, A.N., Adolphs, R., Tyszka, M.J., and O’Doherty, J.P. (2007). Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex. Neuron 55, 545–555.
14. Peters, J., and Buchel, C. (2011). The neural mechanisms of inter-temporal decisionmaking: understanding variability. Trends Cogn. Sci. 15, 227–239.
9. Paton, J.J., Belova, M.A., Morrison, S.E., and Salzman, C.D. (2006). The primate amygdala represents the positive and negative value of
15. Schacter, D.L., and Addis, D.R. (2009). On the nature of medial temporal lobe contributions to the constructive simulation
18. Hernadi, I., Grabenhorst, F., and Schultz, W. (2015). Planning activity for internally generated reward goals in monkey amygdala neurons. Nat. Neurosci. 18, 461–469. 19. Logothetis, N.K. (2008). What we can do and what we cannot do with fMRI. Nature 453, 869–878. 20. Boubela, R.N., Kalcher, K., Huf, W., Seidel, E.M., Derntl, B., Pezawas, L., Nasel, C., and Moser, E. (2015). fMRI measurements of amygdala activation are confounded by stimulus correlated signal fluctuation in nearby veins draining distant brain regions. Sci. Rep. 5, 10499.
Camouflage: Being Invisible in the Open Ocean Thomas W. Cronin Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, MD 21043, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.09.056
Animals inhabiting the open ocean often conceal themselves by being highly transparent, but this transparency is compromised by light that is scattered and reflected from the body surface. New research shows that some midwater crustaceans use antireflection coatings to enhance their invisibility. In sunlit waters of the open ocean, there is literally no place to hide. Animals must conceal themselves in plain sight, using one of the few options available [1]. Silvery fishes with mirror-like scales disappear into the background by reflecting downwardly directed sun light to precisely match the light behind them, effectively cloaking them to visual predators. Silver sides cannot hide any organism seen from below, so many marine animals obliterate their silhouettes using ventral bioluminescence, a phenomenon called counter-illumination. But the mechanism almost universally chosen for small midwater animals is to become completely transparent. Transparency might seem like the perfect solution, but even this has its limitations. If an animal
is to see, its retina must contain lightabsorbing pigments and these create a visible dark spot within the transparent surroundings. A potentially greater problem is that transparent animals, having hard cuticles or even flexible skins, are surrounded by a surface whose refractive index exceeds that of the surrounding water and thus reflects and scatters light from the sun or from the bioluminescent searchlights used by some midwater predators. New research published in this issue of Current Biology by Laura Bagge and her collaborators [2] finds that hyperiid amphipods, predatory crustaceans found throughout the world’s oceans, use anti-reflection coatings to minimize chance reflections, adding a second layer of protection to their already
extreme transparency. Some species may even recruit bacteria to form a biofilm as a component of this magic cloak. Visual predators in the sea look for the chinks in any armor evolved by their prey. For instance, while mirrored sides of shiny fishes offer perfect concealment in principle [3], moving fish inevitably tilt or curl, decreasing the effectiveness of their mirrors. It is also possible that slight mismatches between the polarization of the reflected light and the background polarization might reveal them as well, although this recently has been questioned [4]. Bioluminescent counter-illumination can be defeated by detecting the slight spectral mismatch between the bioluminescent emission spectrum and the background light [5].
Current Biology 26, R1177–R1196, November 21, 2016 Published by Elsevier Ltd. R1179
Current Biology
Dispatches
Figure 1. A portrait of the deep-sea hyperiid amphipod Cystisoma. This creature is about 8–10 cm long and is nearly invisible in life — here it has been carefully lit to show its appearance. Even the sheet-like retinas, which extend over the full surface of the head to search upwardly for prey, are transparent, lacking any absorber other than the reddish visual pigment in photoreceptors. The yellow mass is a brood pouch filled with eggs, which does offer a bit of visual contrast in pregnant females. Otherwise, the combination of outstanding transparency with anti-reflection protuberances and layers of spherical, bacterial nanoplankton on the cuticle makes Cystisoma disappear from view in open water [2]. Photograph by David Liittschwager, used with permission.
Transparency avoids these sorts of problems but introduces others. At one time, polarization vision was thought to defeat transparency because planktonic organisms contain polarization-active materials that alter the polarization of transmitted light, potentially creating background contrast [6]. However, it turns out that polarization is relatively weak in natural waters and that the effect of transparent organisms on this is limited, making it extremely unlikely that polarization vision is able to enhance their visibility [7]. Nevertheless, their transparency is flawed. Most transparent crustaceans, for instance, have welldeveloped compound eyes whose retinas are packed with light-absorbing pigments to maintain optical isolation of retinal photoreceptors. These compact, dark patches are often the only detail that reveals the presence of a transparent organism. (In fact, the tiny retinas of some marine crustacean larvae are hidden by a veil of reflected light matched to the background radiance [8].) Perhaps worse, crustacean cuticles are effective reflectors and scatterers of light, either
downwelling from the sun or moon or from nearby bioluminescence; such scattering can greatly increase the visibility of crustacean zooplankton or other transparent midwater creatures [9]. Similarly, the skin of some deep-sea cephalopods also reflects and scatters light, making them visible even in pitch black surroundings when illuminated by the bioluminescent searchlight of a deep-sea predator. Some cephalopod species quickly expand dark, pigmented chromatophores in their skin in the presence of bioluminescence to minimize such reflections, yet remain transparent the rest of the time to foil predators searching for their silhouettes [10]. One way to counter reflection is to eliminate the refractive index barrier that creates the reflecting surface. Insects do this on the corneas of their compound eyes, covering them with a dense array of tiny projections provokingly called ‘corneal nipples’ [11]. These rounded, paraboloid pillars introduce a gradually increasing bulk refractive index between air and the interior of the cornea, providing no sudden barrier to generate a reflection.
R1180 Current Biology 26, R1177–R1196, November 21, 2016
This produces a slight increase of transparency of the cornea, but the more important effect is that it essentially eliminates reflected glare from the eyes which could reveal the presence of an otherwise camouflaged insect, such as a moth perched on a tree trunk [12]. Could this work in an aquatic environment as well, concealing transparent, not colorcamouflaged, creatures? Enter the hyperiid amphipods (Figure 1). Unlike your typical amphipods, the rather amusing little beach fleas found in driftwood and seaweed on the beach at the high-tide line, the hyperiid amphipods are freely swimming, pelagic predators. They range throughout the world’s oceans, being particularly abundant in nearsurface to upper-mesopelagic waters, and have an unusual life history; most species are symbiotic, parasitic, or commensal on soft-bodied zooplankton (for example, jellies, salps, or siphonophores) at some point in their life cycle [13,14]. Probably the most famous hyperiid is Phronima, a beast that hollows out the body of a salp (a pelagic tunicate), then sits inside and propels itself around like a miniature, submersible jet engine. Phronima’s fame stems from its particularly terrifying appearance, which is said to have inspired the design of the monster in the legendary science-fiction film Alien. However, its hugely expanded ‘braincase’ is actually the optical component of a unique eye, one based on biological fiber optics. In fact, hyperiids are best known to physiologists for the diversity of very weird eye designs they display, many shaped for predation — and avoiding it — in the dim, predictable light of the deep sea [15,16]. Cystisoma’s retina is visible in Figure 1 as the reddish sheets of photoreceptors looking upward in the flattened compound eyes, functioning in the absence of any telltale screening pigment. Many hyperiids are exquisitely transparent, nearly impossible to see when backlit in a laboratory dish or in the open water of the sea. The finest examples of this transparency are the members of the family Cystisomatidae (Figure 1). Without intense, precisely angled lighting, these relatively large animals, reaching well over six inches, are nearly impossible to see. They look like cellophane bags — their water displacement, creating an apparent vacuum in a dish otherwise swarming with
Current Biology
Dispatches plankton, is easier to see than they are. We now know from the new work by Bagge et al. [2] that they add antireflection coatings to this transparency, making them non-reflective as well. In the case of Cystisoma, the legs, and occasionally the carapace itself, are covered with evenly spaced, tapered microprotuberances. When these were carefully measured and then modeled using a variety of theoretical approaches, they were found to reduce surface reflections by some two orders of magnitude (varying with wavelength and angle of incidence). The modeling required estimations of the refractive indices of seawater and chitin, but since these are widely measured elsewhere the outcomes are quite convincing. Having antireflection surfaces on the appendages is particularly useful because these have elevated surface area:volume ratios and move constantly, giving them potentially prominent visibility. Besides Cystisoma’s nanoprotuberances, its cuticle and that of six other hyperiid species (including the fearsome Phronima) were found to be covered with monolayers of small spherical particles. Optical modeling shows that these surface coatings play a similar antireflective role. While the particles have not yet been conclusively identified, indications are that they are nanoplanktonic bacteria that have entered an exosymbiotic relationship with the amphipods, yet another example of the many roles that bacteria have been found to play in the lives of eukaryotes. At this point, measurements of actual reflections from living hyperiids and estimates of their visibility in the sea are lacking. Further, the role of scattering from internal surfaces and structures was not included in the modeled results. Many of these animals occupy forbidding habitats, accessible only by blue-water scuba diving or the use of autonomous or manned submersibles, and anyone who has searched for them in the ocean knows from experience that they are notoriously difficult to see and capture. Specimens captured in deep plankton tows and brought to the surface are usually damaged and often killed, making it difficult to obtain reliable measurements of their visibility. However, the required work will assuredly be done by this team or other future biological oceanographers. Meanwhile, it will be fascinating to learn
how common it is for transparent marine animals to employ antireflection coatings and (in the case of the bacterial symbionts) who exactly it is that coats them. REFERENCES 1. Nilsson, D.-E. (1996). Eye design, vision and invisibility in planktonic invertebrates. In Zooplankton: Sensory Ecology and Physiology, P.H. Lenz, D.K. Hartline, J.E. Purcell, and D.L. Macmillan, eds. (Amsterdam: Gordon and Breach), pp. 149–162.
8. Feller, K.D., and Cronin, T.W. (2014). Hiding opaque eyes in transparent organisms. In situ spectral and image contrast analysis of eyeshine in stomatopod larvae. J. Exp. Biol. 217, 3263–3273. 9. Gagnon, Y.L., Shashar, N., Warrant, E.J., and Johnsen, S. (2007). Light scattering from selected zooplankton from the Gulf of Aqaba. J. Exp. Biol. 210, 3728–3735. 10. Zylinski, S., and Johnsen, S. (2011). Mesopelagic cephalopods switch between transparency and pigmentation to optimize camouflage in the deep. Curr. Biol. 21, 1937– 1941.
2. Bagge, L.E., Osborn, K.J., and Johnsen, S. (2016). Nanostructures and monolayers of spheres reduce surface reflections in hyperiid amphipods. Curr. Biol. 26, 3071–3076.
11. Bernhard, C.G., and Miller, W.H. (1962). A corneal nipple pattern in insect compound eyes. Acta Physiol. Scand. 56, 385–386.
3. Denton, E.J. (1970). On the organization of reflecting surfaces in some marine animals. Phil. Trans. R. Soc. B 258, 285–313.
12. Stavenga, D.G., Foletti, S., Palasantzas, G., and Arikawa, K. (2006). Light on the moth-eye corneal nipple array of butterflies. Proc. R. Soc. B 273, 661–667.
4. Johnsen, S., Gagnon, Y.L., Marshall, N.J., Cronin, T.W., Gruev, V., and Powell, S. (2016). Polarization vision seldom increases the sighting distance of silvery fish. Curr. Biol. 26, R752–R754.
13. Madin, L.P., and Harbison, G.R. (1977). The associations of Amphipoda Hyperiidea with gelatinous zooplankton-I. Associations with Salpidae. Deep-Sea Res. 24, 449–463.
5. Muntz, W.R.A. (1976). On yellow lenses in mesopelagic animals. J. Mar. Biol. Assoc. U.K. 56, 963–976. 6. Shashar, N., Hanlon, R.T., and Petz, A. deM. (1998). Polarization vision helps detect transparent prey. Nature 393, 222–223. 7. Johnsen, S., Marshall, N.J., and Widder, E.A. (2011). Polarization sensitivity as a contrast enhancer in pelagic predators: lessons from in situ polarization imaging of transparent zooplankton. Phil. Trans. R. Soc. B 365, 655–670.
14. Harbison, G.R., Biggs, D.C., and Madin, L.P. (1977). The association of Amphipoda Hyperiidea with gelatinous zooplankton-II. Association with Cnidaria, Ctenophora, and Radiolaria. Deep-Sea Res. 24, 465–488. 15. Land, M.F. (1989). The eyes of hyperiid amphipods: relations of optical structure to depth. J. Comp. Physiol. A 164, 751–762. 16. Fergus, J.L., Johnsen, S., and Osborn, K.J. (2015). A unique apposition compound eye in the mesopelagic hyperiid amphipod Paraphronima gracilis. Curr. Biol. 25, 1–6.
Microbial Evolution: Xenology (Apparently) Trumps Paralogy Laura Eme and W. Ford Doolittle* Department of Biochemistry and Molecular Biology, Dalhousie University, PO Box 15000, Halifax, Nova Scotia B3H 4R2, Canada *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.09.049
Within-genome gene duplication is generally considered the source of extra copies when higher dosage is required and a starting point for evolution of new function. A new study suggests that horizontal gene transfer can appear to play both roles. New genes are generally thought to arise from old genes by the ‘duplication and divergence’ model famously explicated by Susumu Ohno almost fifty years
ago [1]. In this model, one of the duplicates continues to carry out the original function while the other, relieved of that responsibility, is free to mutate and
Current Biology 26, R1177–R1196, November 21, 2016 ª 2016 Elsevier Ltd. R1181
Dispatches 4. Rutishauser, U., Mamelak, A.N., and Adolphs, R. (2015). The primate amygdala in social perception - insights from electrophysiological recordings and stimulation. Trends Neurosci. 38, 295–306. 5. Wang, S., Tudusciuc, O., Mamelak, A.N., Ross, I.B., Adolphs, R., and Rutishauser, U. (2014). Neurons in the human amygdala selective for perceived emotion. Proc. Natl. Acad. Sci. USA 111, E3110–E3119. 6. Grabenhorst, F., Hernadi, I., and Schultz, W. (2012). Prediction of economic choice by primate amygdala neurons. Proc. Natl. Acad. Sci. USA 109, 18950–18955. 7. Haber, S.N., and Knutson, B. (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26.
visual stimuli during learning. Nature 439, 865–870.
of future events. Phil. Trans. R. Soc. Lond. B 364, 1245–1253.
10. Jenison, R.L., Rangel, A., Oya, H., Kawasaki, H., and Howard, M.A. (2011). Value encoding in single neurons in the human amygdala during decision making. J. Neurosci. 31, 331–338.
16. Mosher, C.P., Zimmerman, P.E., and Gothard, K.M. (2014). Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Curr. Biol. 20, 2459–2464.
11. Kim, S., Hwang, J., and Lee, D. (2008). Prefrontal coding of temporally discounted values during intertemporal choice. Neuron 59, 161–172.
17. Chang, S.W., Fagan, N.A., Toda, K., Utevsky, A.V., Pearson, J.M., and Platt, M.L. (2015). Neural mechanisms of social decision-making in the primate amygdala. Proc. Natl. Acad. Sci. USA 112, 16012–16017.
12. Sescousse, G., Redoute, J., and Dreher, J.C. (2010). The architecture of reward value coding in the human orbitofrontal cortex. J. Neurosci. 30, 13095–13104. 13. Bush, G., Luu, P., and Posner, M.I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215–222.
8. Hampton, A.N., Adolphs, R., Tyszka, M.J., and O’Doherty, J.P. (2007). Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex. Neuron 55, 545–555.
14. Peters, J., and Buchel, C. (2011). The neural mechanisms of inter-temporal decisionmaking: understanding variability. Trends Cogn. Sci. 15, 227–239.
9. Paton, J.J., Belova, M.A., Morrison, S.E., and Salzman, C.D. (2006). The primate amygdala represents the positive and negative value of
15. Schacter, D.L., and Addis, D.R. (2009). On the nature of medial temporal lobe contributions to the constructive simulation
18. Hernadi, I., Grabenhorst, F., and Schultz, W. (2015). Planning activity for internally generated reward goals in monkey amygdala neurons. Nat. Neurosci. 18, 461–469. 19. Logothetis, N.K. (2008). What we can do and what we cannot do with fMRI. Nature 453, 869–878. 20. Boubela, R.N., Kalcher, K., Huf, W., Seidel, E.M., Derntl, B., Pezawas, L., Nasel, C., and Moser, E. (2015). fMRI measurements of amygdala activation are confounded by stimulus correlated signal fluctuation in nearby veins draining distant brain regions. Sci. Rep. 5, 10499.
Camouflage: Being Invisible in the Open Ocean Thomas W. Cronin Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, MD 21043, USA Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.09.056
Animals inhabiting the open ocean often conceal themselves by being highly transparent, but this transparency is compromised by light that is scattered and reflected from the body surface. New research shows that some midwater crustaceans use antireflection coatings to enhance their invisibility. In sunlit waters of the open ocean, there is literally no place to hide. Animals must conceal themselves in plain sight, using one of the few options available [1]. Silvery fishes with mirror-like scales disappear into the background by reflecting downwardly directed sun light to precisely match the light behind them, effectively cloaking them to visual predators. Silver sides cannot hide any organism seen from below, so many marine animals obliterate their silhouettes using ventral bioluminescence, a phenomenon called counter-illumination. But the mechanism almost universally chosen for small midwater animals is to become completely transparent. Transparency might seem like the perfect solution, but even this has its limitations. If an animal
is to see, its retina must contain lightabsorbing pigments and these create a visible dark spot within the transparent surroundings. A potentially greater problem is that transparent animals, having hard cuticles or even flexible skins, are surrounded by a surface whose refractive index exceeds that of the surrounding water and thus reflects and scatters light from the sun or from the bioluminescent searchlights used by some midwater predators. New research published in this issue of Current Biology by Laura Bagge and her collaborators [2] finds that hyperiid amphipods, predatory crustaceans found throughout the world’s oceans, use anti-reflection coatings to minimize chance reflections, adding a second layer of protection to their already
extreme transparency. Some species may even recruit bacteria to form a biofilm as a component of this magic cloak. Visual predators in the sea look for the chinks in any armor evolved by their prey. For instance, while mirrored sides of shiny fishes offer perfect concealment in principle [3], moving fish inevitably tilt or curl, decreasing the effectiveness of their mirrors. It is also possible that slight mismatches between the polarization of the reflected light and the background polarization might reveal them as well, although this recently has been questioned [4]. Bioluminescent counter-illumination can be defeated by detecting the slight spectral mismatch between the bioluminescent emission spectrum and the background light [5].
Current Biology 26, R1177–R1196, November 21, 2016 Published by Elsevier Ltd. R1179
Current Biology
Dispatches
Figure 1. A portrait of the deep-sea hyperiid amphipod Cystisoma. This creature is about 8–10 cm long and is nearly invisible in life — here it has been carefully lit to show its appearance. Even the sheet-like retinas, which extend over the full surface of the head to search upwardly for prey, are transparent, lacking any absorber other than the reddish visual pigment in photoreceptors. The yellow mass is a brood pouch filled with eggs, which does offer a bit of visual contrast in pregnant females. Otherwise, the combination of outstanding transparency with anti-reflection protuberances and layers of spherical, bacterial nanoplankton on the cuticle makes Cystisoma disappear from view in open water [2]. Photograph by David Liittschwager, used with permission.
Transparency avoids these sorts of problems but introduces others. At one time, polarization vision was thought to defeat transparency because planktonic organisms contain polarization-active materials that alter the polarization of transmitted light, potentially creating background contrast [6]. However, it turns out that polarization is relatively weak in natural waters and that the effect of transparent organisms on this is limited, making it extremely unlikely that polarization vision is able to enhance their visibility [7]. Nevertheless, their transparency is flawed. Most transparent crustaceans, for instance, have welldeveloped compound eyes whose retinas are packed with light-absorbing pigments to maintain optical isolation of retinal photoreceptors. These compact, dark patches are often the only detail that reveals the presence of a transparent organism. (In fact, the tiny retinas of some marine crustacean larvae are hidden by a veil of reflected light matched to the background radiance [8].) Perhaps worse, crustacean cuticles are effective reflectors and scatterers of light, either
downwelling from the sun or moon or from nearby bioluminescence; such scattering can greatly increase the visibility of crustacean zooplankton or other transparent midwater creatures [9]. Similarly, the skin of some deep-sea cephalopods also reflects and scatters light, making them visible even in pitch black surroundings when illuminated by the bioluminescent searchlight of a deep-sea predator. Some cephalopod species quickly expand dark, pigmented chromatophores in their skin in the presence of bioluminescence to minimize such reflections, yet remain transparent the rest of the time to foil predators searching for their silhouettes [10]. One way to counter reflection is to eliminate the refractive index barrier that creates the reflecting surface. Insects do this on the corneas of their compound eyes, covering them with a dense array of tiny projections provokingly called ‘corneal nipples’ [11]. These rounded, paraboloid pillars introduce a gradually increasing bulk refractive index between air and the interior of the cornea, providing no sudden barrier to generate a reflection.
R1180 Current Biology 26, R1177–R1196, November 21, 2016
This produces a slight increase of transparency of the cornea, but the more important effect is that it essentially eliminates reflected glare from the eyes which could reveal the presence of an otherwise camouflaged insect, such as a moth perched on a tree trunk [12]. Could this work in an aquatic environment as well, concealing transparent, not colorcamouflaged, creatures? Enter the hyperiid amphipods (Figure 1). Unlike your typical amphipods, the rather amusing little beach fleas found in driftwood and seaweed on the beach at the high-tide line, the hyperiid amphipods are freely swimming, pelagic predators. They range throughout the world’s oceans, being particularly abundant in nearsurface to upper-mesopelagic waters, and have an unusual life history; most species are symbiotic, parasitic, or commensal on soft-bodied zooplankton (for example, jellies, salps, or siphonophores) at some point in their life cycle [13,14]. Probably the most famous hyperiid is Phronima, a beast that hollows out the body of a salp (a pelagic tunicate), then sits inside and propels itself around like a miniature, submersible jet engine. Phronima’s fame stems from its particularly terrifying appearance, which is said to have inspired the design of the monster in the legendary science-fiction film Alien. However, its hugely expanded ‘braincase’ is actually the optical component of a unique eye, one based on biological fiber optics. In fact, hyperiids are best known to physiologists for the diversity of very weird eye designs they display, many shaped for predation — and avoiding it — in the dim, predictable light of the deep sea [15,16]. Cystisoma’s retina is visible in Figure 1 as the reddish sheets of photoreceptors looking upward in the flattened compound eyes, functioning in the absence of any telltale screening pigment. Many hyperiids are exquisitely transparent, nearly impossible to see when backlit in a laboratory dish or in the open water of the sea. The finest examples of this transparency are the members of the family Cystisomatidae (Figure 1). Without intense, precisely angled lighting, these relatively large animals, reaching well over six inches, are nearly impossible to see. They look like cellophane bags — their water displacement, creating an apparent vacuum in a dish otherwise swarming with
Current Biology
Dispatches plankton, is easier to see than they are. We now know from the new work by Bagge et al. [2] that they add antireflection coatings to this transparency, making them non-reflective as well. In the case of Cystisoma, the legs, and occasionally the carapace itself, are covered with evenly spaced, tapered microprotuberances. When these were carefully measured and then modeled using a variety of theoretical approaches, they were found to reduce surface reflections by some two orders of magnitude (varying with wavelength and angle of incidence). The modeling required estimations of the refractive indices of seawater and chitin, but since these are widely measured elsewhere the outcomes are quite convincing. Having antireflection surfaces on the appendages is particularly useful because these have elevated surface area:volume ratios and move constantly, giving them potentially prominent visibility. Besides Cystisoma’s nanoprotuberances, its cuticle and that of six other hyperiid species (including the fearsome Phronima) were found to be covered with monolayers of small spherical particles. Optical modeling shows that these surface coatings play a similar antireflective role. While the particles have not yet been conclusively identified, indications are that they are nanoplanktonic bacteria that have entered an exosymbiotic relationship with the amphipods, yet another example of the many roles that bacteria have been found to play in the lives of eukaryotes. At this point, measurements of actual reflections from living hyperiids and estimates of their visibility in the sea are lacking. Further, the role of scattering from internal surfaces and structures was not included in the modeled results. Many of these animals occupy forbidding habitats, accessible only by blue-water scuba diving or the use of autonomous or manned submersibles, and anyone who has searched for them in the ocean knows from experience that they are notoriously difficult to see and capture. Specimens captured in deep plankton tows and brought to the surface are usually damaged and often killed, making it difficult to obtain reliable measurements of their visibility. However, the required work will assuredly be done by this team or other future biological oceanographers. Meanwhile, it will be fascinating to learn
how common it is for transparent marine animals to employ antireflection coatings and (in the case of the bacterial symbionts) who exactly it is that coats them. REFERENCES 1. Nilsson, D.-E. (1996). Eye design, vision and invisibility in planktonic invertebrates. In Zooplankton: Sensory Ecology and Physiology, P.H. Lenz, D.K. Hartline, J.E. Purcell, and D.L. Macmillan, eds. (Amsterdam: Gordon and Breach), pp. 149–162.
8. Feller, K.D., and Cronin, T.W. (2014). Hiding opaque eyes in transparent organisms. In situ spectral and image contrast analysis of eyeshine in stomatopod larvae. J. Exp. Biol. 217, 3263–3273. 9. Gagnon, Y.L., Shashar, N., Warrant, E.J., and Johnsen, S. (2007). Light scattering from selected zooplankton from the Gulf of Aqaba. J. Exp. Biol. 210, 3728–3735. 10. Zylinski, S., and Johnsen, S. (2011). Mesopelagic cephalopods switch between transparency and pigmentation to optimize camouflage in the deep. Curr. Biol. 21, 1937– 1941.
2. Bagge, L.E., Osborn, K.J., and Johnsen, S. (2016). Nanostructures and monolayers of spheres reduce surface reflections in hyperiid amphipods. Curr. Biol. 26, 3071–3076.
11. Bernhard, C.G., and Miller, W.H. (1962). A corneal nipple pattern in insect compound eyes. Acta Physiol. Scand. 56, 385–386.
3. Denton, E.J. (1970). On the organization of reflecting surfaces in some marine animals. Phil. Trans. R. Soc. B 258, 285–313.
12. Stavenga, D.G., Foletti, S., Palasantzas, G., and Arikawa, K. (2006). Light on the moth-eye corneal nipple array of butterflies. Proc. R. Soc. B 273, 661–667.
4. Johnsen, S., Gagnon, Y.L., Marshall, N.J., Cronin, T.W., Gruev, V., and Powell, S. (2016). Polarization vision seldom increases the sighting distance of silvery fish. Curr. Biol. 26, R752–R754.
13. Madin, L.P., and Harbison, G.R. (1977). The associations of Amphipoda Hyperiidea with gelatinous zooplankton-I. Associations with Salpidae. Deep-Sea Res. 24, 449–463.
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Microbial Evolution: Xenology (Apparently) Trumps Paralogy Laura Eme and W. Ford Doolittle* Department of Biochemistry and Molecular Biology, Dalhousie University, PO Box 15000, Halifax, Nova Scotia B3H 4R2, Canada *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.09.049
Within-genome gene duplication is generally considered the source of extra copies when higher dosage is required and a starting point for evolution of new function. A new study suggests that horizontal gene transfer can appear to play both roles. New genes are generally thought to arise from old genes by the ‘duplication and divergence’ model famously explicated by Susumu Ohno almost fifty years
ago [1]. In this model, one of the duplicates continues to carry out the original function while the other, relieved of that responsibility, is free to mutate and
Current Biology 26, R1177–R1196, November 21, 2016 ª 2016 Elsevier Ltd. R1181