Summary and Keywords
Annelid worms are simultaneously an interesting and difficult model system for understanding the evolution of animal vision. On the one hand, a wide variety of photoreceptor cells and eye morphologies are exhibited within a single phylum; on the other, annelid phylogenetics has been substantially re-envisioned within the last decade, suggesting the possibility of considerable convergent evolution. This article reviews the comparative anatomy of annelid visual systems within the context of the specific behaviors exhibited by these animals. Each of the major classes of annelid visual systems is examined, including both simple photoreceptor cells (including leech body eyes) and photoreceptive cells with pigment (trochophore larval eyes, ocellar tubes, complex eyes); meanwhile, behaviors examined include differential mobility and feeding strategies, similarities (or differences) in larval versus adult visual behaviors within a species, visual signaling, and depth sensing. Based on our review, several major trends in the comparative morphology and ethology of annelid vision are highlighted: (1) eye complexity tends to increase with mobility and higher-order predatory behavior; (2) although they have simple sensors these can relay complex information through large numbers or multimodality; (3) polychaete larval and adult eye morphology can differ strongly in many mobile species, but not in many sedentary species; and (4) annelids exhibiting visual signaling possess even more complex visual systems than expected, suggesting the possibility that complex eyes can be simultaneously well adapted to multiple visual tasks.
Annelida is a relatively diverse animal phylum with more than 15,000 described species of segmented worms that exploit a wide array of ecological niches, varying in activity (from motile to sessile), in feeding strategy (e.g., herbivory, detritivory, predation, parasitism, microphagy), and in habitat (from marine to terrestrial) (Struck et al., 2011). Given this considerable diversity of life history strategies, it is not surprising that annelids have adopted a similarly large variety of photoreceptor cells and/or eye morphologies (Figure 1). As a result, annelids have proven an interesting taxon for the study of the evolution of visual systems (for example, see Purschke, Arendt, Hausen, & Muller, 2006). Owing to their simplicity in terms of both their nervous system and behavior, some studies exist that investigate the visual capabilities of annelids (e.g., see Kretz, Stent, & Kristan, 1976; Harley, Cienfuegos, & Wagenaar, 2011; Jékely et al., 2008). However, until now there has not been a study that links the evolution of eyes across annelids to the functional repercussions that this has on their behavior. Here, the available literature is synthesized in an effort to more effectively integrate studies of annelid eye morphology/physiology with those focusing on the underlying behaviors of these animals.
This review chiefly adopts an adaptationist and behavioral approach to examining annelid eye formation, development, and function. It is important, however, to recognize the potential importance of non-adaptive explanations for eye form and function based on evolution by common descent (e.g., Tinbergen’s fourth question; Bateson & Laland, 2013; Tinbergen, 1963). Here there are two non-exclusive reasons why a phylogenetic approach to the questions posed here is less emphasized (at this time): (1) the recent challenging and revision of annelid relationships and (2) issues surrounding well-documented evidence for the deep homology of animal eyes.
Traditionally, two classes of Annelida have been recognized based on morphology: Polychaeta, which often possess numerous setae and paired appendages (parapodia) per body segment; and Clitellata (earthworms, leeches, and kin), in which parapodia are lacking and a clitellum functions in cocoon formation during direct development (Brusca & Brusca, 2003; Purschke, Bleidorn, & Struck, 2014; Rouse & Fauchald, 1997). The initial cladistic analyses based on morphology suggested a sister group relationship between Polychaeta and Clitellata, with two major clades of polychaetes recognized (Palpata and Scolecida) (Purschke et al., 2014; Rouse & Fauchald, 1997). In the 2000s, however, molecular phylogenetic studies drastically altered our view of this phylum (e.g., McHugh, 2000; Struck et al., 2007, 2011; Weigert et al., 2014). Weigert and Bleidorn (2016) recently reviewed annelid phylogeny, summarizing the following key insights (Figure 2): (1) inclusion of Sipuncula and Echiura (previously classified at the phylum level); (2) paraphyly of Polychaeta; and (3) the re-establishment, with modification, of the two formerly recognized clades Sedentaria (Clitellata, Echiura, and “polychaetes” commonly adapted to burrow or tube-living) and Errantia (“polychaetes” that often actively crawl or swim; e.g., nereids), as well as five basal taxa (Sipuncula, Amphinomidae, Chaetopteridae, Magleonidae, and Oweniidae).
Not surprisingly, in light of these changes in our view of annelid evolution, substantial evidence for convergent morphological evolution has been discovered in the phylum. For example, the four known toxin/venom-producing annelid taxa are found throughout the phylum: one basally, one in Errantia, and two in different lineages of Sedentaria (Struck, 2017). Other clear examples of homoplasy in the annelid phylogeny include convergent use of terrestrial and lake habitats, independent evolution of microscopic taxa from macroscopic taxa, and repeated instances of body plan simplification and character loss (including reduction in segmentation) (reviewed by Weigert & Bleidorn, 2016). In this vein, Purschke and colleagues have repeatedly questioned the utility of solely using various visual structures in the resolution of the phylogenetic position of annelids at both higher (e.g., adult eye structures of Errantia within the Lophotrochozoa; Suschenko & Purschke, 2008) and lower taxonomic levels (e.g., placement of Polygordius based on its photoreceptor-like sense organs; Lehmacher, Ramey-Balci, Wolff, Fiege, & Purschke, 2016; Wilkens & Purschke, 2009). This suggests that it remains too early to develop a strong thesis regarding the evolutionary history of annelid visual systems.
Finally, and more generally, the metazoan eye presents another challenge to phylogenetic studies: it is literally a textbook example of deep homology (Futuyma, 2013). Studies of the pax gene family (notably the Pax6 subfamily in Bilateria) have uncovered the possibility of an ancient molecular “toolkit” underlying photoreception, including the remarkable ability of deuterostome and cnidarian Pax family genes to induce “ectopic” eye formation in Drosophila (Halder, Callaerts, & Gehring, 1995; Suga et al., 2010). This suggests that, while the morphological structures of the eye are certainly capable of convergently evolving (e.g., the camera type eyes of cephalopod mollusks and vertebrates), the underlying developmental components of vision are present and highly conserved across animals (Vopalensky & Kozmik, 2009). From an evolutionary-developmental perspective, therefore, it would not be unreasonable to expect some convergence in eye morphology and function (but not necessarily in developmental origin), especially within a large phylum expressing a wide diversity of life histories and visual structures.
If not from a phylogenetic perspective, then what is the context in which a review of annelid vision will be examined? Here, a more functional approach is taken to analyzing annelid vision by examining trends that lead to increased functionality of the visual system, followed by any behavioral capabilities these functional changes confer onto individuals. These trends in the evolution of eyes were beautifully described in Nilsson (2009) and will be summarized here and in Figure 3. The simplest form of visual sensor would be a single cell able to transduce light. This cell would not sense much in terms of changes in luminosity, nor would it be able to sense directionality of the light source, leading to limitations in its capability to direct behaviors. These visual sensors would not be for orientation to a stimulus, but rather could allow circadian entrainment or perhaps enable burrowing animals to assess their level of exposure. The next step in complexity would be membrane stacking in the form of microvilli (in the case of rhabdomeric photoreceptor cells) or cilia (in the case of ciliary photoreceptor cells). This would allow a 2–3 log unit gain in sensitivity and the ability to sense differences in luminosity. An animal with this sort of photoreceptor cell would now be able to perhaps sense time of day or its depth within an aquatic environment. Next would come the addition of a screening pigment that would aid with the receptor’s ability to sense the directionality of light, as it would block out light coming from certain directions. This basic structure of photoreceptor cell and a supportive cell with shading pigment has long been thought to represent the simplest structure able to be called an eye (Darwin, 1859; Richter et al., 2010). If an animal had multiple photoreceptor cells coupled with a pigment layer, it would be able to receive spatial information in addition to directional information from the light (Nilsson, 2009). The last addition to eye complexity would be the addition of a lens that would enable the eye to capture more photons and would add focusing power. At any point in this process, the visual sensor can exhibit duplications, evolving more photoreceptor cells, something that can also aid in the effectiveness of the eye for different visual tasks. Using Nilsson’s framework, annelid vision can be examined at each of these key innovations in terms of both the underlying anatomy and the behaviors they allow for. This is the first time that annelid vision has been examined from this perspective.
Part I: Anatomy
To understand the capabilities of the annelid visual system, one must first understand the anatomy underlying it, starting with an examination of the photoreceptor cells, and then progressing to more and more complex visual structures (summarized in Figure 4). It is important to note that annelids exhibit a large diversity in eye type and number (Table 1). Furthermore, in species with indirect development, the larvae often exhibit eyes that are completely different from those of the adult.
Table 1. Summary of Photoreceptor and Eye Types Found in Adults of Featured Annelid Species
Notes: The Latin binomial for each species refers to that used in the referenced study and may not represent the currently accepted nomenclature. +, present; -, absent; ?, unknown; P = phaosomal receptor.
In the past it was hypothesized that photoreceptor cells belonged in one of two categories, ciliary or rhabdomeric, depending on the orientation and origin of their membranous folds (Eakin, 1963, 1979). It was thought that by investigating the evolutionary origins of these photoreceptor cell types a deeper understanding of phylogeny and the evolutionary origins of visual structures could be achieved. This very division was used in an attempt to clarify various phylogenies (including that of the annelids), and shortly after being proposed it generated opponents. Even its own proposer, Eakin, stated, “the erection of a system of pigeon holes usually presents a problem of what to do with the pigeon that does not fit any of the holes” (Eakin, 1972, p. 653). Annelids proved to occupy a key position in this debate. There are several factors that made the annelids Eakin’s “pigeon.” The most notable of these is the phaosomal photoreceptor cell, present in Clittellata (e.g., leeches), which do not fit in either category. Did these receptors evolve from the ciliary or rhabdomeric subtypes, or did they evolve from something new altogether? While there is still some debate, current morphological and molecular data strongly suggest a rhabdomeric origin for phaosomal photoreceptors (Döring et al., 2013). From a functional perspective, these phaosomal photoreceptor cells have fewer membranous folds than their ciliary or rhabdomeric counterparts, which could influence their sensitivity to different luminosities. Outside of clitellates, phaosomal photoreceptors are rare; however, there are still roadblocks to using the ciliary or rhabdomeric classification. Many annelids have a vestigial cilium in their rhabdomeric photoreceptor cells, thought to be an artifact of the photoreceptor cell itself evolving from a locomotor cilium (Arendt & Wittbrodt, 2001; Arendt, Hausen, & Purschke, 2009). Furthermore, those annelids that exhibit this character often exhibit both ciliary and rhabdomeric photoreceptor cell types (Purschke, 2005; Purschke et al., 2006). Due to this redundancy, light sensitivity to the ciliary photoreceptive cells has been questioned; however, Arendt and colleagues revealed that, in Platynereis dumerilii, the opsins are present to allow these cells to transduce light (Arendt, Tessmar-Raible, Snyman, Dorresteijn, & Wittbrodt, 2004).
Why are there two types of photoreceptors? Arendt et al. (2009) proposed that it is for a “division of labor”; ciliary photoreceptors in the body wall lack photopigment and are thus involved in non-directional tasks such as withdrawal responses to light or regulation of circadian rhythms, while rhabdomeric photoreceptors are most often located on the head of the animal and accompanied by pigment allowing them to guide behaviors that require directional sensitivity (Arendt et al., 2009; Nilsson & Arendt, 2008; Purschke, 2005).
Photoreceptor Cells as Visual Sensors
Here, photoreceptor cells occurring without being accompanied by a pigment cell are examined. In some clitellates photoreceptor cells are distributed within the epithelium of the epidermis and do not co-occur with supporting pigment cells, and thus are only capable of sensing light and dark. The greatest concentration of these often occurs on the prostomium (Hesse, 1897; Röhlich, Aros, & Vrágh, 1970). These photoreceptor cells fall into a category called extraocular photoreceptor cells (EOCs), which have uncharacterized functions at this time. EOCs may occur in animals with complex eyes or visual sensilla, and do occur in the leeches Hirudo verbana, Helobdella stagnalis, and Helobdella robusta (which have both) (Clark, 1967; Döring et al., 2013; Kretz et al., 1976). In H. verbana, EOCs are phaosomal and look identical to the photoreceptor cells of the complex eye. Dermal light cells or EOCs often do not even fall within traditional definitions of an eye or even a photoreceptor cell (Ramirez, Speiser, Pankey, & Oakley, 2011); however, they have been shown to mediate behavioral responses across many taxa, such as shadow and withdrawal responses in some gastropods (Crisp, 1972; Stoll, 1972, 1973) and brittle stars (Hendler & Byrne, 1987), phototaxis in Platyneris larvae (Jékely et al., 2008), and dermal coloration in cephalopods (Packard & Brancato, 1993). In annelids, these cells have also been shown to mediate withdrawal reflexes, escape, and orientation along the dorso-ventral axis and are present in both clitellates and polychaetes (Backfisch et al., 2013; Drewes & Fourtner, 1989; Jellies, 2014a; Purschke, Hugenschütt, Ohlmeyer, Meyer, & Weihrauch, 2017). Other than the potential for these receptors to mediate withdrawal responses, very little is known about them or their capability.
Aggregations of Photoreceptor Cells
Body Eyes or Visual Sensilla
In addition to the lone extraocular photoreceptor cells, leeches also exhibit aggregations of photoreceptor cells distributed on their body wall. These sensilla (sometimes also referred to as the “body eyes”) exhibit a multitude of cell types including mechanoreceptive cilia, chemoreceptive cells, and four phaosomal photoreceptive cells (Phillips & Friesen, 1982; Whitman, 1886). These photoreceptor cells are not accompanied by a pigment cell and thus would not be able to sense directionality. Leeches have a large number of these sensilla, with most of the leech’s 21 segments having anywhere from 2 to 7 pairs (Derosa & Friesen, 1981; Fernández, Téllez, & Olea, 1992; Hesse, 1897; Sawyer, 1986). Interestingly, Whitman, who first characterized these sensors in Hirudo medicinalis, noted that those on the dorsal surface of the animal were larger than those on the ventral surface, which may have functional implications (see below) (Whitman, 1886). What is perhaps most intriguing about these visual sensilla in Hirudo verbana is that they connect to nerves, which carry sensory information to the leech’s ganglion. This would make them both dispersed and higher-order photoreceptor cells (see Ramirez et al., 2011), a combination not before noted in studies of extraocular photoreceptor cells and one that could imbue them with more functionality than has been noted in other animals. In addition, their regular and yet distributed pattern of organization would seem far more than is necessary to entrain circadian cycles or assess exposure levels.
Photoreceptive Cells Coupled With Pigment
Larval Eyes in Polychaetes
Larval eyes in annelids are among the most simple in the animal kingdom, consisting of often only two cells: a supportive cell with shading photopigment (PSC) and a photoreceptive cell (PRC) (Arendt et al., 2009; Jékely et al., 2008; Purschke et al., 2006) (Fig. 4C). In this case, the sensory processes projecting from the eyes most often project away from incoming light, leading to this type of eye being referred to as having an “inverse” structure (Purschke et al., 2006; Schmidt-Rhaesa, Harzsch, & Purschke, 2016). While possession of this eye design does not seem like it would provide much in the functional sense, Platynereis larvae are able to exhibit phototactic behavior even when only one of their two eye spots is intact (Jékely et al., 2008).
The addition of more photoreceptor cells to such an eye would increase its sensitivity to changes in light levels; therefore, one might suspect that the adult eyes of Platynereis dumerilii are simply a larval version that has had more photoreceptor cells added to it throughout development. This is not the case, however; while the adult eyes do have more photoreceptor cells, their eyes arise from a completely different developmental process (Arendt et al., 2009). This perhaps leads to a more interesting scenario whereby two different developmental processes have converged on similar solutions for a visual system.
Ocellar tubes are among the simplest of eyes. Their photoreceptor cells, which are few in number, co-occur with pigment cells. These exist on the brain surface and receive their signal from the outside through a long tube filled with a cuticular plug (Purschke, 2011). While this plug could have a lens-like effect, additional projections of muscles and cilia into the cuticular plug could make the ocellar tube sense mechanical deformation as well as light, giving it a multimodal functionality (Purschke, 2011).
Typical adult eyes are often more complex than those of larvae, consisting of more photoreceptor cells and both pigmented and unpigmented support cells. Additionally, the sensory processes of adult eyes are usually “everse” (projecting toward the light), whereas those of larvae are inverse (projecting away) (Suschenko & Purschke, 2008). However, complexity varies greatly across the annelids, with some lacking eyes, some having eyes with few photoreceptor cells, and others having an additional accessory retina and special focusing mechanisms in their eye (Purschke et al., 2006; Randel & Jékely, 2016; Wald & Rayport, 1977).
Across clitellates, the anatomical ground plan for the complex eyes is similar. Eyes are only found in Hirudinea (which are carnivorous or ectoparasitic) and in limnetic Naidinae (which live in shallow plant cover within ponds) among the oligochaetes (Purschke, 2003; Sawyer, 1986; Stephenson, 1930). These eyes (often referred to as “cephalic eyes” in leeches) are created by several layers of phaosomal receptors similar to those found within the epidermis and visual sensilla (Clark, 1967; Döring et al., 2013; Yanase, Fujimoto, & Nishimura, 1965). Here they are located within a surrounding pigment layer; this is unlike the photoreceptor cells found elsewhere on the body (Fernández et al., 1992; Jamieson, 1992; Purschke, 2003). This layering of photoreceptor cells would add additional sensitivity to changes in luminosity. The addition of the pigment cup surrounding the photoreceptor cells would only allow light from specific directions to enter the eye, allowing it to sense the directionality of the stimulus. While the basic structure is similar across leeches, species vary in their number, size, and the location of their cephalic eyes (a trait that has been used to identify them in the field) (Mann, 1923; Sawyer, 1986).
Most eyes in polychaetes consist of an epithelial layer composed of pigment and sensory cells forming a cup-like depression covered by unpigmented cells (Suschenko & Purschke, 2008). The microvilli from the sensory cells project into the inner part of the cup (the optical cavity). Beyond this basic ground plan, there is exceptional diversity in the number and location of eyes and the number of photoreceptor cells in a given eye; in addition, many species have unique taxon-specific adaptations. It should be noted, however, that not all polychaetes have eyes; some species have incredibly reduced photoreceptor cells, some have complex eyes, and some have no eyes at all.
Part II: Behavior
It is clear that there is a large diversity of structures underlying the anatomy of annelid vision (see Figs. 1 and 4). While the functional limitations of the anatomy from the theoretical construct must be understood, to truly understand it the behavioral functionality of animals exhibiting each visual morphology must also be examined.
Simple Photoreceptor Cells
Here the behavioral capabilities of animals using the simplest photoreceptor cells present in the annelids are examined, starting with phaosomal receptors (see above). These cellular photoreceptor systems lack the screening pigments needed to fully sense the direction of the light source. Below are a few model systems in which light induced behaviors have been studied and could be guided by these simple sensors.
The Earthworm: Lumbricus terrestris
It has been known since the time of Darwin that annelids exhibit a photokinesis, a non-directional response to light. Darwin noted that the subterranean Lumbricus terrestris would withdraw back into its burrow when exposed to sudden changes in luminosity (Darwin, 1881), with larger changes in luminosity magnifying the response. This withdrawal response also depends on the location in which light contacts its body; only light contacting the worm’s anterior evokes robust withdrawal responses (Darwin, 1881). In his writings, Darwin was somewhat mystified by these responses because these animals “do not possess eyes but can distinguish between light and darkness.” It is now known that what guides these responses is not an “eye,” but rather a series of phaosomal photoreceptor cells unaccompanied by a pigment cell. Further examination of these withdrawal responses revealed that they are context dependent, suggesting more complexity than a simple reflex. For example, worms moved toward weak sources of light but away from strong sources of light (Doolittle, 1972). Ongoing behavioral events could further modulate the worm’s response—it was diminished if the worm was eating, dragging leaves into its burrow, or engaged in copulation (Darwin, 1881). Indeed, it was later discovered that this modulation of the response appears to be under the control of the supraesophageal ganglion (Blue, 1976). In a related species, Eisenia foetida, lesion studies found that removal of the connection between the brain and nerve cord diminished the response to light; however, 4 days following lesion, the nervous system had recovered enough for functionality to return (note that these results are regarded by some as controversial; see Blue, 1976; Prosser, 1934). Either way, it would seem that, unlike a simple reflex, these behaviors are controlled by higher order systems that can modulate the gain of the response depending on the environmental context.
The Visual Sensilla of the Leech
Leeches have phaosomal receptors not unlike those found in earthworms. While some of these phaosomal receptors occur alone and concentrated on the leech’s anterior and posterior suckers, as in Lumbricus, the majority of them are regularly arranged in small groupings within multimodal sensilla. There are 14 of these multimodal sensilla on each of the leech’s 21 segments. While these sensilla are capable of initiating a light-based withdrawal response, additional functions that seem to be related to the regular distribution of these sensilla are noted here. For instance, differences in the sensitivity of the dorsal and ventral sensilla to UV stimulation may help the leech to sense its own body orientation while swimming (Jellies, 2014a, 2014b). Furthermore, leeches can also sense differences between anterior stimulation (which causes a “head withdrawal”) and posterior stimulation (which causes a “tail withdrawal”) (Jellies, 2014a). Taken together, these observations suggest that the nervous system can compare signals from these 294 visual sensilla in a spatial manner (Jellies, 2014a, 2014b). Indeed, they are able to localize the sources of water waves using visual stimuli, but it is not known whether this is guided by the sensilla or the cephalic eyes (Dickinson & Lent, 1984; Harley et al., 2011). The sensilla become a factor in determining which prey animal is being tracked, something important in this species, Hirudo verbana, which switches their preferred prey with age (Sawyer, 1986). This prey switch is mediated by their sensitivity to different wave frequencies (Harley et al., 2011). How is this modulated? As the leeches age their sensilla gain both more afferents and sensory hairs, which biases this multimodal sensor more toward mechanosensory stimuli and away from visual stimuli (Gascoigne & McVean, 1993; Harley et al., 2011; Peinado, Zipser, & Macagno, 1990). Thus, while these visual sensilla are indeed simple, they may find complexity in numbers, enabling them to extrapolate some spatial information by detecting the location of a stimulus on the leech. If combined with a population code, it could be possible for these very simple visual sensors to direct visually oriented behaviors in the leech; however, more investigation is required to see if this is the case.
How are these body wall sensilla capable of sensing directionality without the use of a screening pigment? One possibility is that an alternative pigment is being used to block light. Annelids have extracellular hemoglobin, and leeches often have a stomach full of blood containing hemoglobin, a pigment with light-absorbing capabilities. It is possible that hemoglobin blocks light from some directions, allowing the sensilla to be more directionally sensitive than they would be in the absence of pigment. Note that while this may seem farfetched, the same mechanism has been found to underlie visual localization in the nematode Mermis nigrescens (Mohamed, Burr, & Burr, 2007).
Polychaete Extraocular Photoreceptor Cells
The polychaetes Platynereis dumerilii and Branchiomma vesiculosum have been shown to exhibit a robust light avoidance response following eye removal or decapitation (Backfisch et al., 2013; Hesse, 1897). This suggests that, in these polychaetes, light avoidance responses are led by photoreceptors located outside of the complex eyes (Backfisch et al., 2013). These photoreceptor cells, also found in opheliid and sabellid polychaetes, are found in groupings on each of the segments of the worm, similar to the sensilla in the leech (Derosa & Friesen, 1981; Salvani-Plawen & Mayr, 1977). Given what is known about earthworms, it would be easy for simple photoreceptors to mediate a withdrawal response; however, with photoreceptor cells on each segment the possibility remains that these polychaetes (as with leeches) may be capable of more than a simple withdrawal response by using the numerical complexity of these simple cellular photoreceptor arrays.
At first glance, this extra functionality would seem redundant and wasteful—especially in animals that have very few neurons to process visual information. One possibility of avoiding this issue is that the two photosensory structures retain entirely different behavioral functions. It has been suggested that there is a division in function between complex eyes and extraocular photoreceptor cells; eyes respond to visual motion, and the extraocular photoreceptor cells respond to shadow (Nicol, 1950). These strategies are likely not “one size fits all”; some species could divide functions among the photoreceptor cell groups in a manner different from other species. For example, while Platynereis dumerilii lives within a transparent tube, in sabellids these tubes are opaque making any sort of body eye less likely to be exposed—much less to respond to shadow. Other annelids live in dense environments where shadows would be unlikely during day-to-day life. Furthermore, they might not all need to withdraw. Do these animals possess these photoreceptor cells in case they find themselves outside of their normal environment? Or do these photoreceptor cells guide an alternate behavioral function (e.g., training circadian rhythms or dorso-ventral orientation)? More research is needed to determine the functionality of these photoreceptor cells across different annelids. Through functional segregation of the different visual systems, it is possible that less neural processing is needed to initiate an appropriate response to a stimulus. Furthermore, having many simple sensors in an array would allow for some of that processing to be offloaded from the primary neurons to the sensory array, an option that matches with the numerically simple nervous systems present in annelids.
Simple Photoreceptor Cells Coupled with Screening Pigment
Ocellar Tubes of Sipunculids
Sipunculids exhibit a single pair of ocellar tubes, which correspond structurally to the adult eyes present in polychaetes (see “Part I: Anatomy”), each having a few photoreceptor cells (Hermans & Eakin, 1969). These annelids burrow and use tentacles to passively collect food items (Fine, Sabbah, Shashar, & Hoegh-Guldberg, 2013). While their ocelli are known to elicit a withdrawal reflex, little is known about other visual behaviors they possess (Peebles & Fox, 1933). A similar eye exists in the polychaete, Fauveliopsis adriatica, which has also been found to have several projections from presumed stretch receptors (making the structure appear to be multimodal) (Purschke, 2005, 2011). It is possible that a similar multimodality could be true of the sipunculid ocellar tube. Thus, although the role of ocellar tubes in behavior is not well understood and more investigation into their sensory capabilities is needed, it would seem unlikely that an animal with two such simple eyes would be able to do much more than use light to detect whether or not it was in its burrow or perhaps entrain a circadian clock.
Larval Eyes of Polychaetes
Despite the fact that it would seem that a mere pair of very simple eyes (as seen in sipunculids) would not exhibit much of a navigational function, the larval eyes of Platynereis dumerilii may make us question this assertion. These larvae have a single pair of simple “proto-eyes” composed of a single photoreceptor cell attached to a supporting pigment cell (Jékely et al., 2008). Each two-celled eye has a direct connection to a locomotor ciliary cell (Randel et al., 2014). Light shining on one of these photoreceptor cells modulates the beating of the cilia, steering the animal (Jékely et al., 2008). This allows them to move toward the light during the types of vertical migration typical of zooplankton (Thorson, 1964). This very simple neural circuit is thought to be a rather large first step in the evolution of visual systems (Arendt et al., 2009). Additional such small circuits could allow for finer control of direction of movement (see Braitenberg, 1986). Amazingly, Platynereis larvae are able to orient toward light when only a single photoreceptor cell is intact. Of course, if both are ablated they lose their orientation ability entirely (Jékely et al., 2008).
It is important to note that these larvae are not solely guided by visual stimuli; these could be combined with sensation of other environmental stimuli to better guide their responses and even allow for a greater complexity in response. Phragmatopoma lapidosa exhibits a similar phototactic behavior in the larval state to Platynereis dumerilii; however, it is coupled with a geotaxis, which changes sign over the course of the animal’s life. One-day-old larvae show a positive phototaxis and (a much weaker) positive geotaxis, which would direct them to the surface and the largest abundance of their phytoplankton food during the day and downward at night (McCarthy, Forward, & Young, 2002). The involvement of these senses in feeding behavior is further supported by the modulation of this phototaxis by their level of satiety; hungry larvae are more positively phototactic than sated larvae. By day 5, however, the geotaxis is no longer present in these animals and they switch to a negative phototaxis, resulting in an optimal position in the water column for dispersal. At 28 days they exhibit a coupled negative phototaxis and positive geotaxis, which is thought to help them to descend at night, eventually settling on the bottom where they will live as adults (McCarthy et al., 2002). A similar interplay between phototaxis and geotaxis is found in another sedentary polychaete (Serpula vermicularis), potentially indicating a pattern (Young & Chia, 1982). Many sedentary polychaetes exhibit larval eyes even into adulthood, which perhaps speaks to simple eyes filling functional needs to direct and maintain burrowing behavior.
Cephalic Eyes of Hirudo verbana
If an animal with two eyes—each only consisting of a photoreceptor cell and a pigment cell—can direct an animal through its environment, then what behaviors are possible when the animal is equipped with a greater number of photoreceptor cells? Hirudo verbana has cephalic eyes consisting of numerous phaosomal receptors layered within a pigment cup in addition to visual sensilla and extraocular photoreceptor cells (see “Part I: Anatomy”). While often not thought of as being visual animals, leeches are able to localize prey using solely visual stimuli (although in nature mechanosensory and chemical stimuli also play a role in guiding this behavior) (Dickinson & Lent, 1984; Harley et al., 2011, Harley, Rossi, Cienfuegos, & Wagenaar, 2013; Young, Dedwylder, & Friesen, 1981). Here, motion created through scanning and crawling movements aids the leech in better localization of prey within their environment by creating additional visual and mechanosensory cues (Harley et al., 2013; Harley & Wagenaar, 2014). When mechanosensory stimuli are removed, leeches are still able to localize prey, suggesting that vision plays a role in this complex behavior (Dickinson & Lent, 1984; Harley et al., 2011). Additionally, in the leech Hirudo verbana the relative importance of these stimuli to prey localization changes during development to potentially help the leech localize an appropriate food source for that developmental stage (Harley et al., 2011). So what exactly are leeches sensing that indicates nearby prey? It is suspected that leeches respond to changes in luminosity created as water waves make temporary lenses on the surface, focusing the light on the substrate below (caustics).
The visual sensors responsible for prey localization remain unknown. Depending on the species, leeches may have up to 10 cephalic eyes, each having up to 50 phaosomal photoreceptor cells each and 294 visual sensilla. Preliminary experiments suggest that leeches with the nerves innervating the cephalic eyes cut were no longer able to visually localize prey (Cynthia M. Harley, unpublished observation). While it is not completely clear whether the visual sensilla or the cephalic eyes are used to guide this behavior, the anatomy suggests that the structure of the eye (which includes multiple layers of photoreceptor cells and a screening pigment) should prove adequate to the task. It is intriguing that these cephalic eyes occur in different numbers and positions in different leech species (see above), and it is possible that this represents differential adaptation to each species’ environment and prey. No matter why it occurs, the fact that the eyes occupy different head regions will undoubtedly change how the animal perceives its environment. Current studies are investigating the behavioral capability of leech cephalic eyes, with particular emphasis on differences occurring across species with different ecological niches.
The Complex Eyes of Adult Polychaetes
Some annelid visual systems would almost appear to be overbuilt. This is the case with the polychaetes Sabella melanostigma and Dasychone conspersa, which both exhibit a light-induced withdrawal reflex. Both species have large numbers of eyes, with S. melanostigma exhibiting 240 eyes with each having 60 ommatidia (Nilsson, 1994). This would appear to be far more eyes that necessary for a simple withdrawal reflex—so why are so many eyes present? One possibility discussed earlier is that this reduces the amount of computation needed by the nervous system, something perhaps especially important to animals with so few neurons (Nilsson, 1994). Second, this large eye number allows for the animal to better discriminate between an actual predator and something that could occlude a simple photoreceptor cell without posing a threat (e.g., a planktonic organism) (Nilsson, 1994). A similar strategy is noted in locusts whereby a stimulus must subtend a certain number of ommatidia to elicit a collision avoidance response (Hatsopoulos, Gabbiani, & Laurent, 1995). Third, the number of eyes would allow these tube-living worms to better detect threats under conditions of low contrast and low sensitivity; this is likely especially important for S. melanostigma, which lives in the turbid waters of mangrove streams (Nilsson, 1994). Finally, if the eyes serve as an alarm system, damage by predators would result in decreased surveillance capacity; thus, the large number of eyes could compensate for this (Nilsson, 1994). Whatever the reason, these animals have the ability to sense an object that only subtends 0.75° of the visual field. To put this into perspective, one’s thumb held at arm’s length subtends 2° of the visual angle, which exceeds the visual acuity of most insects (Land, 1997; O’Shea, 1991). Here, the continuation of a trend present in many annelids is noted: the ability to compensate for the simplicity of their individual eyes by having many eyes, giving them similar complexity and resolution to a single, more complex eye. Perhaps in future studies of visual systems, researchers should investigate not only eye complexity but also the complexity of visual scene that comes with an increase in sensor number.
Visual Communication in Annelids
In addition to prey localization and predator avoidance, some annelids have shown an ability to communicate with conspecifics through the use of visual signals. One example, the Bermuda fireworm (Odontosyllis enpola), is a polychaete that emits a bioluminescent signal during courtship. Here, females at the water surface begin to exhibit a bioluminescent signal down the entire length of their body; which attracts males from more than 4.5m away whom respond by flashing intermittently in response (Galloway & Welch, 1911). This species has two pairs of eyes consisting of a lens, pigment cup, and an array of photoreceptor cells arranged in sheets backed by photopigment. Males, the intended receivers, have larger eyes than females. These eyes exhibit two peak responses to light wavelengths: one from 420–430 nm and another around 510–520 nm (Nicol, 1978; Wilkens & Wolken, 1981). The female signal courtship signal emission occurs between 507 and 516 nm (Nicol, 1978; Shimomura, Johnson, & Saiga, 1963). In addition to their peak sensitivities, the eyes of the fireworm have additional adaptations to increase their behavioral capability: (1) a greater-than-usual folding within the photoreceptor cell and (2) a particular lens arrangement. The folding or membrane stacking increases the sensitivity of the eye to different light intensities (Nilsson, 2009). The lens is created out of a series of tubes aligned with the optical axis, allowing the lens to guide the light into the eye not unlike a fiber optic, increasing its ability to guide orientation behavior (Wolken & Florida, 1984).
The retina of the fireworm has two peak sensitivities; while one clearly corresponds to the female signal, what does the other correspond to? While it could perceive UV light and indicate time of day (see below), there is another possibility seen in another marine polychaete, Tomopteris septentrionalis, that also uses a bioluminescent signal to detect mates (Dales, 1971). This species has been found to escape from the flashing bioluminescent signal of dinoflagellates (approximated at 475 nm for 60 ms duration) (Buskey & Swift, 1985). While this signal is likely used by dinoflagellates for protection, it could mimic a predator or an unresponsive mate and result in the polychaete’s turn and rapid swim away from its source. Indeed, accounts of T. septentrionalis bioluminescence suggest that it is greener when they have been disturbed and bluer during the natural behavior.
Spectral information would appear important for communication; however, it could also have another use. For aquatic annelids, light can provide information about depth or time of day; however, these are not easily distinguished because dim light could indicate either a deeper location or that it is later in the day. Without a spectral comparison of the light composition, the two signals are indistinguishable (Lythgoe, 1979; Nilsson, 2009). Torrea candida, a deep sea alcopiid, has been found to have two retinas, each differing in peak sensitivity. Potentially, the peak sensitivity of the primary retina (400 nm, corresponding to UV light) would make an excellent sensor for time of day (Wald & Rayport, 1977). The accessory retina, on the other hand, has a peak sensitivity of 560 nm, a wavelength that dissipates rapidly in deep water, and thus could serve as an effective depth gauge (Wald & Rayport, 1977).
In this article the key insights, highlighted based on a review of morphological form and behavioral function in annelid visual systems, are as follows.
More mobile adult polychaetes exhibit more complex eyes than those that are sedentary (Purschke & Nowak, 2015), and those with a more predatory life cycle also exhibit increased visual complexity. Given the large division in annelid taxonomy between Errantia and Sedentaria, this may have both an adaptive and a phylogenetic basis. Examples of this are seen in the predatory alcopiids which have large eyes containing many photoreceptor cells and are thought to be image forming (Eakin & Hermans, 1988; Wald & Rayport, 1977). Conversely, benthic polychaetes have reduced eyes or no eyes at all (Giere, 2013). Examination of the tube-dwelling polychaetes in the family Serpulidae reveals that some individuals are active feeders and some are passive suspension feeders (Jumars, Dorgan, & Lindsay, 2015). Perhaps it is not strange to note that some serpulids have simple eyes and others complex eyes, with the eye location being highly variable. Further research is needed, but it is likely that annelids that take a more active role in feeding would exhibit either a more complex eye or a greater number of simple eyes.
Annelid visual systems have the potential to use simple sensors toward more complex ends. First, many annelids have a multitude of very simple eyes, something which may capitalize on distributed sensing to both decrease neural processing needs and to increase visual resolution. Second, some annelid visual sensors may also be involved in detecting stimuli in other modalities (e.g., mechanoreception). Both of these adaptations may lead to more efficient perception and/or processing of information from the environment. Furthermore, this combination of a multimodal sensor that is visual has not been found in other animals, and yet many animals integrate visual information with other modalities. It would be interesting to examine the benefits of an “all-in-one” system. The efficiency of information perception allowed by these adaptations would be particularly important in animals with a relatively limited number of neurons.
Sensors of different modalities can combine their information in different ways as animals mature. The modulation of how each modality relates to the other can have extraordinary behavioral effects. Examples in the annelids include Platynereis dumerilii, which changes the interrelation between phototaxis and geotaxis to match the behavioral needs of each life stage, and the leech Hirudo verbana, which also exhibits a similar change in relation between mechanosensory and visual inputs, something that influences the prey it is best able to sense at different times during its development. This is particularly notable as in Platynereis dumerilii this change occurs during the trochophore larval stage, whereas the leech lacks a larval stage suggesting that similar strategies can be exhibited during very different developmental processes.
In polychaetes possessing a trochophore larva, eye form and function can be considerably different than those of the eventual adult. This is not always the case, however, with many sedentary species retaining larval eyes, or at least larval eye morphology, into adulthood. This throws caution to assumptions that animals with complete metamorphosis necessarily have strongly divorced sensory needs and underscores another key difference between Errantia and Sedentaria.
Annelids that exhibit visual signaling (e.g., fireworms) possess complex eyes, as expected, although the sensitivity of the visual system is not necessarily tuned solely to conspecific signals. Studies of other systems suggest the possibility of predator-avoidance behavior or measurement of time of day/depth perception as alternative adaptive benefits.
In conclusion, past and current studies of annelid vision reveal interesting relationships between form and function—some that are reasonably expected based on the animal’s behavioral repertoire and others that suggest potential mismatches between eye and behavioral complexity. Further research into the capabilities of even highly simplified structures will be key to understanding the tremendous diversity of annelid visual systems. Finally, more research into the phylogenetic relationships of annelids is needed, so that adaptive explanations can be more readily divorced from potential constraints due to shared evolutionary history.
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