- Email: [email protected]
Visual Ecology: Now You See, Now You Don’t
Current Biology
Dispatches Visual Ecology: Now You See, Now You Don’t Daniel R. Chappell and Daniel I. Speiser* Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.12.002
During the day, the brittle star Ophiocoma wendtii demonstrates spatial vision due to a distributed network of extraocular photoreceptors whose fields of view are restricted by chromatophores. At night, these chromatophores contract and O. wendtii loses spatial vision. Animals have evolved diverse methods for obtaining spatial information about light [1]. The most familiar approach to spatial vision is for an animal to have a pair of image-forming eyes on its head. Examples of these visual systems include the compound eyes of arthropods and the camera-type eyes of vertebrates and cephalopods. A less familiar approach to spatial vision is for an animal to have numerous light-sensing structures spread across its body. The separate lightsensing structures that contribute to these distributed visual systems vary in location, abundance, and complexity. Sea urchins (Figure 1A), for example, gather spatial information about light using thousands of photoreceptors distributed across their orb-shaped bodies [2,3]. Other animals with distributed visual systems gather spatial information about light using lesser numbers of more complex lightsensing structures. Sabellid (Figure 1B) and serpulid polychaetes, for example, have hundreds of small compound eyes on their radioles, the specialized tentacles they use for gas-exchange and filter-feeding [4,5]. Among molluscs, chitons (Figure 1C) have hundreds of small camera-type eyes embedded in their shell plates [6] and scallops (Figure 1D) have dozens of eyes with mirror-based optics on the edges of their mantles [7]. In two recent papers, one of which is published in this issue of Current Biology, Sumner-Rooney and colleagues expand our knowledge of distributed visual systems by describing how a species of brittle star, Ophiocoma wendtii (Figure 1E), obtains spatial information about light using thousands of extraocular photoreceptors dispersed across its five segmented arms [8,9]. Restricting the fields of view of separate photoreceptors
is necessary for spatial vision and O. wendtii accomplishes this task using pigmented cells termed chromatophores [9]. When these chromatophores are in their expanded state, the spatial acuity demonstrated by O. wendtii in behavioral trials (30–50 ) is consistent with the solid angles over which their individual photoreceptors collect light (30–40 ). One lesson from brittle stars is that biological structures with interesting optical properties are not necessarily used by animals for optical functions. Previous authors proposed that O. wendtii collects light for
photoreception using the numerous lensshaped calcitic structures, termed enlarged peripheral trabeculae (EPTs), that are embedded in its arms [10]. Sumner-Rooney and colleagues argue convincingly, however, that the EPTs in O. wendtii do not contribute to spatial vision. Instead of lying underneath the EPTs and receiving focused light from above, the photoreceptors associated with vision in O. wendtii are found in pores surrounding the EPTs [8,9]. Another lesson from O. wendtii is that distributed visual systems composed of extraocular photoreceptors can be
Figure 1. Animals with distributed visual systems. (A) The sea urchin Diadema africanum demonstrates spatial vision despite lacking eyes (photo credit: J.C. Herna´ndez); (B) the sabellid fan worm Bispira melanostigma has pairs of compound eyes (visible here as dark dots) on the radioles it uses for filter-feeding (photo credit: M.J. Bok); (C) the chiton Acanthopleura granulata has small camera-type eyes embedded in its shell plates (photo credit: D. Liittschwager); (D) the bay scallop Argopecten irradians has mirror-based eyes along the edges of its valves (photo credit: D. Liittschwager); (E) the brittle star Ophiocoma wendtii demonstrates spatial vision thanks to a network of extraocular photoreceptors dispersed across its five segmented arms (photo credit: L. SumnerRooney).
Current Biology 30, R64–R91, January 20, 2020 ª 2019 Elsevier Ltd. R71
Current Biology
Dispatches A
B
Current Biology
Figure 2. The light-influenced contraction and expansion of chromatophores alters visual acuity in the brittle star Ophiocoma wendtii. (A) In the dark, the chromatophores contract, the photoreceptors have fields of view of 118 deg and acceptance angles of 54 deg, and animals do not orient to spatial cues. (B) In the light, the chromatophores expand, the photoreceptors have fields of view of 68 deg and acceptance angles of 31 deg, and animals orient to spatial cues.
dynamic. The eyes of many animals have pupils that constrict in the light and dilate in the dark. These pupillary responses modulate trade-offs between resolution and sensitivity to optimize the performance of visual systems under variable light conditions [11]. In O. wendtii, the functional consequences of a pigment-based pupillary response are particularly dramatic [9]. In the light, the chromatophores surrounding the photoreceptors expand, the fields of view of the photoreceptors narrow, and animals orient their movements to spatial cues (Figure 2). In the dark, the chromatophores contract, the fields of view of the photoreceptors broaden, and animals do not orient their movements to spatial cues. Why does O. wendtii, unlike any other animal yet described, maximize light-gathering power at night to the point that it sacrifices spatial vision entirely? By comparing the visual abilities of multiple species of brittle star, SumnerRooney and colleagues demonstrate that closely related taxa can differ in whether or not they have spatial vision. Like its congener O. wendtii, the brittle star O. pumila detects light using a distributed network of thousands of extraocular photoreceptors [8]. Unlike O. wendtii, O. pumila lacks chromatophores and does not demonstrate spatial vision [9]. If the ability to gather spatial information about light differs between congeners like O. wendtii and O. pumila, it suggests spatial vision may evolve rapidly and frequently. In the case of Ophiocoma, the
evolution of spatial vision is linked to the origin of an association between photoreceptors and light-responsive chromatophores, a relatively simple evolutionary step compared to others proposed in stepwise models of eye evolution [12]. Comparing the visual systems and light-influenced behaviors of additional species of brittle star, in a phylogenetically-informed context, will help shed light on how rapidly and how frequently spatial vision may evolve. Comparisons between the sympatric O. wendtii and O. pumila raise the possibility that differences in spatial vision may contribute to niche-partitioning. If so, differences in sensory ecology could help maintain the coexistence of otherwise similar species within a single habitat. Both O. wendtii and O. pumila forage in open areas, but they respond differently when exposed to light. The species with spatial vision, O. wendtii, seeks shelter under rocks or in larger crevices, whereas the species without spatial vision, O. pumila, seeks smaller crevices or buries itself [13]. Thus, differences in spatial vision between species with similar foraging behaviors may lead to these species seeking separate microhabitats for shelter. An intriguing question is whether differences in shelter-seeking behavior between species of Ophiocoma evolved before or after the origin of spatial vision in the genus. Put more broadly, do changes in behavior tend to drive changes in sensory systems or do changes in sensory
R72 Current Biology 30, R64–R91, January 20, 2020
systems tend to drive changes in behavior? Just as animals with distributed visual systems employ diverse light-sensing structures, they also process information about light in diverse ways. Sea urchins, for example, almost certainly process spatial information about light in a decentralized manner because they have a decentralized nervous system with hundreds of small ganglia [14]. Chitons, in comparison, may process spatial information in a centralized or decentralized manner: a recent study proposes they have a brain, but we have yet to learn if this neural structure helps process visual information [15]. Compared to other animals with distributed visual systems, fan worms and scallops take centralized approaches to visual processing. In fan worms, the processing of visual information is likely centralized because afferent fibers descending from the eyebearing radioles project to the supraesophogeal ganglion [16]. In scallops, optic nerves from the majority of the eyes on the mantle travel directly to lobes that are part of the parietovisceral ganglion [17]. Further characterization of sensory processing in O. wendtii and other brittle stars will help us learn how and why animals with distributed visual systems take different approaches to processing spatial information about light. To understand how animals with distributed visual systems convert sensory input into behavioral output, we must investigate their sensory-motor circuits. Comparisons between O. wendtii and O. pumila are a promising opportunity to test if small changes in sensory input are sufficient to cause differences in behavior or if changes in the underlying sensory-motor circuits are necessary. Historically, it was thought that brittle stars and other echinoderms use their circumoral nerve ring as a behaviorcontrol center. However, recent evidence suggests that every segment in a brittle star’s arm acts as a sensory-motor unit and that these sensory-motor units form a network whose actions are under decentralized control [18,19]. If brittle stars use a decentralized control scheme, their coordinated whole-body behaviors must result from interactions between these sensory-motor units. In other
Current Biology
Dispatches words, if we want to understand lightmediated behaviors in brittle stars, we must understand processing within their sensory-motor units and communication across their entire sensory-motor network. Using conventional neuroethological approaches, it can be challenging to understand how behaviors are produced by decentralized sensory-motor networks. As an alternative approach, we may better understand visually influenced behaviors in brittle stars if we approximate individual animals as a swarm. Swarms can be conceptualized as collections of semi-autonomous agents acting under decentralized control. They often exhibit emergent behaviors that extend beyond the behaviors that can be performed by a single agent [20]. The sensory-motor units of brittle stars may be considered agents: they function semi-autonomously due to sparse neural connectivity and they send and receive global signals via a giant neuron pathway that is present in all five arms and the central disc [14]. One functional advantage of a swarm is that its behavior is robust to the loss of individual agents [20]. Brittle stars exhibit just this sort of robustness — they can accommodate for the loss of arm segments, single arms, or even multiple arms by altering their locomotory behaviors [19]. Given these discoveries, we will gain insight into the engineering of robust sensory-motor networks through further work on brittle stars and other animals with distributed visual systems. REFERENCES
6. Speiser, D.I., Eernisse, D.J., and Johnsen, S. (2011). A chiton uses aragonite lenses to form images. Curr. Biol. 21, 665–670. 7. Land, M.F. (1965). Image formation by a concave reflector in the eye of the scallop, Pecten maximus. J. Physiol. 179, 138–153. 8. Sumner-Rooney, L., Rahman, I.A., Sigwart, J.D., and Ullrich-Lu¨ter, E. (2018). Whole-body photoreceptor networks are independent of ‘lenses’ in brittle stars. Proc. R. Soc. B 285, 20172590. 9. Sumner-Rooney, L., Kirwan, J.D., Lowe, E., and Ullrich-Lu¨ter, E. (2020). Extraocular vision in a brittle star is mediated by chromatophore movement in response to ambient light. Curr. Biol. 30, 319–327. 10. Aizenberg, J., Tkachenko, A., Weiner, S., Addadi, L., and Hendler, G. (2001). Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412, 819. 11. Laughlin, S.B. (1992). Retinal information capacity and the function of the pupil. Ophthalmic Physiol. Opt. 12, 161–164. 12. Nilsson, D.-E. (2013). Eye evolution and its functional basis. Vis. Neurosci. 30, 5–20. 13. Sides, E.M., and Woodley, J.D. (1985). Niche separation in three species of Ophiocoma (Echinodermata: Ophiuroidea) in Jamaica. West Indies. Bull. Mar. Sci. 36, 701–715. 14. Cobb, J.L.S. (1995). The nervous systems of Echinodermata: recent results and new
approaches. In The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach (Springer), pp. 407–424. 15. Sumner-Rooney, L., and Sigwart, J.D. (2018). Do chitons have a brain? New evidence for diversity and complexity in the polyplacophoran central nervous system. J. Morphol. 279, 936–949. 16. Orrhage, L. (1980). On the structure and homologues of the anterior end of the polychaete families Sabellidae and Serpulidae. Zoomorphology 96, 113–167. 17. Spagnolia, T., and Wilkens, L.A. (1983). Neurobiology of the scallop. II. Structure of the parietovisceral ganglion lateral lobes in relation to afferent projections from the mantle eyes. Mar. Behav. Physiol. 10, 23–55. 18. Zueva, O., Khoury, M., Heinzeller, T., Mashanova, D., and Mashanov, V. (2018). The complex simplicity of the brittle star nervous system. Front. Zool. 15, 1. 19. Clark, E.G., Kanauchi, D., Kano, T., Aonuma, H., Briggs, D.E., and Ishiguro, A. (2019). The function of the ophiuroid nerve ring: how a decentralized nervous system controls coordinated locomotion. J. Exp. Biol. 222, jeb192104. 20. Garnier, S., Gautrais, J., and Theraulaz, G. (2007). The biological principles of swarm intelligence. Swarm Intell. 1, 3–31.
Supergene Evolution: Recombination Finds a Way Brendan G. Hunt Department of Entomology, University of Georgia, Griffin, GA 30223, USA Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.12.006
1. Land, M.F., and Nilsson, D.-E. (2012). Animal Eyes (Oxford: Oxford University Press). 2. Kirwan, J.D., Bok, M.J., Smolka, J., Foster, J.J., Herna´ndez, J.C., and Nilsson, D.-E. (2018). The sea urchin Diadema africanum uses low resolution vision to find shelter and deter enemies. J. Exp. Biol. 221, jeb176271. 3. Yerramilli, D., and Johnsen, S. (2010). Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). J. Exp. Biol. 213, 249–255. 4. Bok, M.J., Capa, M., and Nilsson, D.-E. (2016). Here, there and everywhere: the radiolar eyes of fan worms (Annelida, Sabellidae). Integr. Comp. Biol. 56, 784–795. 5. Bok, M.J., Porter, M.L., Ten Hove, H.A., Smith, R., and Nilsson, D.-E. (2017). Radiolar eyes of serpulid worms (Annelida, Serpulidae): structures, function, and phototransduction. Biol. Bull. 233, 39–57.
Supergenes are multiple linked genes that regulate complex, polymorphic traits, but little is known about their evolution. A new study of an ancient supergene in several ant species suggests that rare recombination events shape supergene evolution in surprising ways. Chromosomal inversions have long garnered attention from geneticists. Studies on Drosophila flies in the mid-20th century demonstrated that inversions reduce the frequency of recombination between homologous chromosomes on which genes are arranged in inverted order. Dobzhansky and Epling noted in 1948 that, ‘‘inversion is therefore a
powerful means of holding together gene combinations which confer upon their carriers superior adaptive properties’’ [1]. Recombination suppression by chromosomal inversion plays a key role in the evolution of heteromorphic sex chromosome systems [2,3], and sex dimorphism provides an archetypal example of complex trait polymorphism.
Current Biology 30, R64–R91, January 20, 2020 ª 2019 Elsevier Ltd. R73
Dispatches Visual Ecology: Now You See, Now You Don’t Daniel R. Chappell and Daniel I. Speiser* Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.12.002
During the day, the brittle star Ophiocoma wendtii demonstrates spatial vision due to a distributed network of extraocular photoreceptors whose fields of view are restricted by chromatophores. At night, these chromatophores contract and O. wendtii loses spatial vision. Animals have evolved diverse methods for obtaining spatial information about light [1]. The most familiar approach to spatial vision is for an animal to have a pair of image-forming eyes on its head. Examples of these visual systems include the compound eyes of arthropods and the camera-type eyes of vertebrates and cephalopods. A less familiar approach to spatial vision is for an animal to have numerous light-sensing structures spread across its body. The separate lightsensing structures that contribute to these distributed visual systems vary in location, abundance, and complexity. Sea urchins (Figure 1A), for example, gather spatial information about light using thousands of photoreceptors distributed across their orb-shaped bodies [2,3]. Other animals with distributed visual systems gather spatial information about light using lesser numbers of more complex lightsensing structures. Sabellid (Figure 1B) and serpulid polychaetes, for example, have hundreds of small compound eyes on their radioles, the specialized tentacles they use for gas-exchange and filter-feeding [4,5]. Among molluscs, chitons (Figure 1C) have hundreds of small camera-type eyes embedded in their shell plates [6] and scallops (Figure 1D) have dozens of eyes with mirror-based optics on the edges of their mantles [7]. In two recent papers, one of which is published in this issue of Current Biology, Sumner-Rooney and colleagues expand our knowledge of distributed visual systems by describing how a species of brittle star, Ophiocoma wendtii (Figure 1E), obtains spatial information about light using thousands of extraocular photoreceptors dispersed across its five segmented arms [8,9]. Restricting the fields of view of separate photoreceptors
is necessary for spatial vision and O. wendtii accomplishes this task using pigmented cells termed chromatophores [9]. When these chromatophores are in their expanded state, the spatial acuity demonstrated by O. wendtii in behavioral trials (30–50 ) is consistent with the solid angles over which their individual photoreceptors collect light (30–40 ). One lesson from brittle stars is that biological structures with interesting optical properties are not necessarily used by animals for optical functions. Previous authors proposed that O. wendtii collects light for
photoreception using the numerous lensshaped calcitic structures, termed enlarged peripheral trabeculae (EPTs), that are embedded in its arms [10]. Sumner-Rooney and colleagues argue convincingly, however, that the EPTs in O. wendtii do not contribute to spatial vision. Instead of lying underneath the EPTs and receiving focused light from above, the photoreceptors associated with vision in O. wendtii are found in pores surrounding the EPTs [8,9]. Another lesson from O. wendtii is that distributed visual systems composed of extraocular photoreceptors can be
Figure 1. Animals with distributed visual systems. (A) The sea urchin Diadema africanum demonstrates spatial vision despite lacking eyes (photo credit: J.C. Herna´ndez); (B) the sabellid fan worm Bispira melanostigma has pairs of compound eyes (visible here as dark dots) on the radioles it uses for filter-feeding (photo credit: M.J. Bok); (C) the chiton Acanthopleura granulata has small camera-type eyes embedded in its shell plates (photo credit: D. Liittschwager); (D) the bay scallop Argopecten irradians has mirror-based eyes along the edges of its valves (photo credit: D. Liittschwager); (E) the brittle star Ophiocoma wendtii demonstrates spatial vision thanks to a network of extraocular photoreceptors dispersed across its five segmented arms (photo credit: L. SumnerRooney).
Current Biology 30, R64–R91, January 20, 2020 ª 2019 Elsevier Ltd. R71
Current Biology
Dispatches A
B
Current Biology
Figure 2. The light-influenced contraction and expansion of chromatophores alters visual acuity in the brittle star Ophiocoma wendtii. (A) In the dark, the chromatophores contract, the photoreceptors have fields of view of 118 deg and acceptance angles of 54 deg, and animals do not orient to spatial cues. (B) In the light, the chromatophores expand, the photoreceptors have fields of view of 68 deg and acceptance angles of 31 deg, and animals orient to spatial cues.
dynamic. The eyes of many animals have pupils that constrict in the light and dilate in the dark. These pupillary responses modulate trade-offs between resolution and sensitivity to optimize the performance of visual systems under variable light conditions [11]. In O. wendtii, the functional consequences of a pigment-based pupillary response are particularly dramatic [9]. In the light, the chromatophores surrounding the photoreceptors expand, the fields of view of the photoreceptors narrow, and animals orient their movements to spatial cues (Figure 2). In the dark, the chromatophores contract, the fields of view of the photoreceptors broaden, and animals do not orient their movements to spatial cues. Why does O. wendtii, unlike any other animal yet described, maximize light-gathering power at night to the point that it sacrifices spatial vision entirely? By comparing the visual abilities of multiple species of brittle star, SumnerRooney and colleagues demonstrate that closely related taxa can differ in whether or not they have spatial vision. Like its congener O. wendtii, the brittle star O. pumila detects light using a distributed network of thousands of extraocular photoreceptors [8]. Unlike O. wendtii, O. pumila lacks chromatophores and does not demonstrate spatial vision [9]. If the ability to gather spatial information about light differs between congeners like O. wendtii and O. pumila, it suggests spatial vision may evolve rapidly and frequently. In the case of Ophiocoma, the
evolution of spatial vision is linked to the origin of an association between photoreceptors and light-responsive chromatophores, a relatively simple evolutionary step compared to others proposed in stepwise models of eye evolution [12]. Comparing the visual systems and light-influenced behaviors of additional species of brittle star, in a phylogenetically-informed context, will help shed light on how rapidly and how frequently spatial vision may evolve. Comparisons between the sympatric O. wendtii and O. pumila raise the possibility that differences in spatial vision may contribute to niche-partitioning. If so, differences in sensory ecology could help maintain the coexistence of otherwise similar species within a single habitat. Both O. wendtii and O. pumila forage in open areas, but they respond differently when exposed to light. The species with spatial vision, O. wendtii, seeks shelter under rocks or in larger crevices, whereas the species without spatial vision, O. pumila, seeks smaller crevices or buries itself [13]. Thus, differences in spatial vision between species with similar foraging behaviors may lead to these species seeking separate microhabitats for shelter. An intriguing question is whether differences in shelter-seeking behavior between species of Ophiocoma evolved before or after the origin of spatial vision in the genus. Put more broadly, do changes in behavior tend to drive changes in sensory systems or do changes in sensory
R72 Current Biology 30, R64–R91, January 20, 2020
systems tend to drive changes in behavior? Just as animals with distributed visual systems employ diverse light-sensing structures, they also process information about light in diverse ways. Sea urchins, for example, almost certainly process spatial information about light in a decentralized manner because they have a decentralized nervous system with hundreds of small ganglia [14]. Chitons, in comparison, may process spatial information in a centralized or decentralized manner: a recent study proposes they have a brain, but we have yet to learn if this neural structure helps process visual information [15]. Compared to other animals with distributed visual systems, fan worms and scallops take centralized approaches to visual processing. In fan worms, the processing of visual information is likely centralized because afferent fibers descending from the eyebearing radioles project to the supraesophogeal ganglion [16]. In scallops, optic nerves from the majority of the eyes on the mantle travel directly to lobes that are part of the parietovisceral ganglion [17]. Further characterization of sensory processing in O. wendtii and other brittle stars will help us learn how and why animals with distributed visual systems take different approaches to processing spatial information about light. To understand how animals with distributed visual systems convert sensory input into behavioral output, we must investigate their sensory-motor circuits. Comparisons between O. wendtii and O. pumila are a promising opportunity to test if small changes in sensory input are sufficient to cause differences in behavior or if changes in the underlying sensory-motor circuits are necessary. Historically, it was thought that brittle stars and other echinoderms use their circumoral nerve ring as a behaviorcontrol center. However, recent evidence suggests that every segment in a brittle star’s arm acts as a sensory-motor unit and that these sensory-motor units form a network whose actions are under decentralized control [18,19]. If brittle stars use a decentralized control scheme, their coordinated whole-body behaviors must result from interactions between these sensory-motor units. In other
Current Biology
Dispatches words, if we want to understand lightmediated behaviors in brittle stars, we must understand processing within their sensory-motor units and communication across their entire sensory-motor network. Using conventional neuroethological approaches, it can be challenging to understand how behaviors are produced by decentralized sensory-motor networks. As an alternative approach, we may better understand visually influenced behaviors in brittle stars if we approximate individual animals as a swarm. Swarms can be conceptualized as collections of semi-autonomous agents acting under decentralized control. They often exhibit emergent behaviors that extend beyond the behaviors that can be performed by a single agent [20]. The sensory-motor units of brittle stars may be considered agents: they function semi-autonomously due to sparse neural connectivity and they send and receive global signals via a giant neuron pathway that is present in all five arms and the central disc [14]. One functional advantage of a swarm is that its behavior is robust to the loss of individual agents [20]. Brittle stars exhibit just this sort of robustness — they can accommodate for the loss of arm segments, single arms, or even multiple arms by altering their locomotory behaviors [19]. Given these discoveries, we will gain insight into the engineering of robust sensory-motor networks through further work on brittle stars and other animals with distributed visual systems. REFERENCES
6. Speiser, D.I., Eernisse, D.J., and Johnsen, S. (2011). A chiton uses aragonite lenses to form images. Curr. Biol. 21, 665–670. 7. Land, M.F. (1965). Image formation by a concave reflector in the eye of the scallop, Pecten maximus. J. Physiol. 179, 138–153. 8. Sumner-Rooney, L., Rahman, I.A., Sigwart, J.D., and Ullrich-Lu¨ter, E. (2018). Whole-body photoreceptor networks are independent of ‘lenses’ in brittle stars. Proc. R. Soc. B 285, 20172590. 9. Sumner-Rooney, L., Kirwan, J.D., Lowe, E., and Ullrich-Lu¨ter, E. (2020). Extraocular vision in a brittle star is mediated by chromatophore movement in response to ambient light. Curr. Biol. 30, 319–327. 10. Aizenberg, J., Tkachenko, A., Weiner, S., Addadi, L., and Hendler, G. (2001). Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412, 819. 11. Laughlin, S.B. (1992). Retinal information capacity and the function of the pupil. Ophthalmic Physiol. Opt. 12, 161–164. 12. Nilsson, D.-E. (2013). Eye evolution and its functional basis. Vis. Neurosci. 30, 5–20. 13. Sides, E.M., and Woodley, J.D. (1985). Niche separation in three species of Ophiocoma (Echinodermata: Ophiuroidea) in Jamaica. West Indies. Bull. Mar. Sci. 36, 701–715. 14. Cobb, J.L.S. (1995). The nervous systems of Echinodermata: recent results and new
approaches. In The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach (Springer), pp. 407–424. 15. Sumner-Rooney, L., and Sigwart, J.D. (2018). Do chitons have a brain? New evidence for diversity and complexity in the polyplacophoran central nervous system. J. Morphol. 279, 936–949. 16. Orrhage, L. (1980). On the structure and homologues of the anterior end of the polychaete families Sabellidae and Serpulidae. Zoomorphology 96, 113–167. 17. Spagnolia, T., and Wilkens, L.A. (1983). Neurobiology of the scallop. II. Structure of the parietovisceral ganglion lateral lobes in relation to afferent projections from the mantle eyes. Mar. Behav. Physiol. 10, 23–55. 18. Zueva, O., Khoury, M., Heinzeller, T., Mashanova, D., and Mashanov, V. (2018). The complex simplicity of the brittle star nervous system. Front. Zool. 15, 1. 19. Clark, E.G., Kanauchi, D., Kano, T., Aonuma, H., Briggs, D.E., and Ishiguro, A. (2019). The function of the ophiuroid nerve ring: how a decentralized nervous system controls coordinated locomotion. J. Exp. Biol. 222, jeb192104. 20. Garnier, S., Gautrais, J., and Theraulaz, G. (2007). The biological principles of swarm intelligence. Swarm Intell. 1, 3–31.
Supergene Evolution: Recombination Finds a Way Brendan G. Hunt Department of Entomology, University of Georgia, Griffin, GA 30223, USA Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.12.006
1. Land, M.F., and Nilsson, D.-E. (2012). Animal Eyes (Oxford: Oxford University Press). 2. Kirwan, J.D., Bok, M.J., Smolka, J., Foster, J.J., Herna´ndez, J.C., and Nilsson, D.-E. (2018). The sea urchin Diadema africanum uses low resolution vision to find shelter and deter enemies. J. Exp. Biol. 221, jeb176271. 3. Yerramilli, D., and Johnsen, S. (2010). Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). J. Exp. Biol. 213, 249–255. 4. Bok, M.J., Capa, M., and Nilsson, D.-E. (2016). Here, there and everywhere: the radiolar eyes of fan worms (Annelida, Sabellidae). Integr. Comp. Biol. 56, 784–795. 5. Bok, M.J., Porter, M.L., Ten Hove, H.A., Smith, R., and Nilsson, D.-E. (2017). Radiolar eyes of serpulid worms (Annelida, Serpulidae): structures, function, and phototransduction. Biol. Bull. 233, 39–57.
Supergenes are multiple linked genes that regulate complex, polymorphic traits, but little is known about their evolution. A new study of an ancient supergene in several ant species suggests that rare recombination events shape supergene evolution in surprising ways. Chromosomal inversions have long garnered attention from geneticists. Studies on Drosophila flies in the mid-20th century demonstrated that inversions reduce the frequency of recombination between homologous chromosomes on which genes are arranged in inverted order. Dobzhansky and Epling noted in 1948 that, ‘‘inversion is therefore a
powerful means of holding together gene combinations which confer upon their carriers superior adaptive properties’’ [1]. Recombination suppression by chromosomal inversion plays a key role in the evolution of heteromorphic sex chromosome systems [2,3], and sex dimorphism provides an archetypal example of complex trait polymorphism.
Current Biology 30, R64–R91, January 20, 2020 ª 2019 Elsevier Ltd. R73