Male eyes Apollo, Nyx the female eyes
Stearn’s Wharf, the landmark wooden pier that effectively extends Santa Barbara’s main drag of State Street 1900 feet into the Pacific, is usually crowded with sightseers, diners, and fishermen; locals and tourists alike. Yet, unless they enter the Sea Center, probably very few of the visitors to the wharf stop and consider what is living just meters below the wooden pier where they walk. The ostracod crustacean species Euphilomedes morini is one of these denizens of the not-so-deep, and because of its distinctive eyes, it is an object of scientific study within the Cheadle Center for Biodiversity and Ecological Restoration at the University of California-Santa Barbara. Euphilomedes morini males have compound eyes that would make proud Apollo, the Greek God of light. But females lack these eyes, nixed not by the Goddess of night (Nyx), but by evolution and development.
Fig. 1 - Stearn's Wharf, Santa Barbara, CA
Before discussing E. morini and its eyes, I will first introduce the class of animals to which the species belongs, Ostracoda, the ostracod crustaceans. Ostracods are small and ancient crustaceans, usually the size of sesame seeds or smaller. Sometimes known as “seed shrimp”, they make their debut in the fossil record in deposits of Ordovician Age, rocks that are some 450 million years old. Following this ancient appearance, ostracods are notoriously abundant in the fossil record. In some places, ostracod density can reach up to several thousand individuals per 100 g (3.5 oz) rock mass!
In addition to the estimated 30,000 different fossil ostracod species, some 15,000 species are alive today. But only roughly half of these living ostracods are known to science (have official scientific names). On one research expedition to a marine lab in Puerto Rico, I dipped a bucket in the ocean and chanced to find an unknown species, which we later named Euphilomedes chupacabra. This was on the pier of the marine lab, where hundreds of marine biologists have walked, and where their boats are docked. If unknown species live here, imagine what remains to be discovered in the farthest depths of the oceans, or the remotest ponds and pools. Even the subject of this piece, E. morini was first named as recently as 1997, after Jim Morin, an ostracodologist who has contributed much to our knowledge of the “fireflies of the sea”, a family of ostracods whose males produce brilliant blue light flashes to attract females (those females have eyes).
Ostracods are not confined to oceans. They live almost anywhere there is water. The small temporary ponds (vernal pools) that fill with California’s winter rains are home to hundreds of ostracod species. Life stages are resistant to drying over California’s long and often rainless summers. On a hike in the foothills above Montecito one winter, I once found a crevice in a boulder that had filled with rain water. To my surprise, that tiny bit of water teemed with ostracods. These animals also live in the water filled cups of bromeliad flowers, and some species even live without standing water, for example in the damp leaf litter of Australian rainforests, and just above the tides in the United Kingdom.
Not surprisingly, given the diversity of habitats occupied by ostracods, different species make a living in a wide variety of different ways. Some ostracods are scavengers. Others are predators, like the “giant” deep sea ostracod, Gigantocypris. Almost the size of a ping pong ball, Gigantocypris uses large silvery reflectors to focus light on its tiny retina and track down prey like plankton and even small fishes. Many ostracods are “deposit feeders”, feeding indiscriminately on organic matter found on the bottom of oceans or lakes.
Like the common housefly, ostracods are arthropods. Both houseflies and some ostracods see the world using compound eyes. Unlike our own eyes, which focus light through a single lens like a camera, compound eyes sample light through many lenses each a part of a separate facet called an ommatidium. Housefly compound eyes have hundreds of facets, while ostracod eyes have at most about 60, but usually fewer. Interestingly most living ostracods lack compound eyes, but some have them.
Euphilomedes moriniAlthough many ostracod species live locally, one in particular has been the subject of research in our lab for two reasons. First, E. morini is quite common and easily collected from Stearn’s Wharf or Goleta Pier. We simply drop a grab-sampler into the the water and bring up a bit of sand from the bottom of the Pacific. E. morini is one of the commonest animals of its size (~1 mm) in the shallow waters of the California coast. Second, E. morini has an interesting feature: Males have large compound eyes, but females do not.
Figure 2 (A, B) Lateral view of adult animals with half of carapace removed. Anterior is to the left. One lateral eye is visible (arrows). The female eye (A) is small and rudimentary without ommatidia and is only faintly pigmented. The male eye (B) is much larger, dominating the head of the animal with clearly visible ommatidia and a small rudiment (arrowhead) (C, D, E). Lateral view of instar IV male eyes from Euphilomedes longiseta (C) and Euphilomedes morini (D) and instar V Euphilomedes carcharodonta. Arrowheads denote rudiments. Stage matched lateral eyes from these three species are indistinguishable. Panel (E) depicts the development of a male compound eye. Pigment was photobleached under UV to allow a better view of the morphology. All rudiment pigmentation was removed in the photobleaching. The largest lenses and darkest pigmentation are at the distal end of the ommatidial field. Growth appears to occur in the direction of the curved arrow, as suggested by the presence of smaller lenses and fainter pigmentation. A putative morphogenic front is marked with a red arrowhead. (F, G) Eyes of late stage embryos (carapace fully formed) of the cylidroleberid Postasterope barnesi (F) and E. carcharodonta (G). Ommatidia are forming in the cylindroleberid embryo (arrows) but are absent in E. carcharodonta. (H, I) Ommatidial structure of E. morini. The schematic is based on panel (H), DAPI nuclear staining, and previous data on ostracod eyes (Land and Nilsson 1990). The distal portion of the ommatidia is the two lenses, which are clear and highly autofluorescent. These overlie two pigment cells (P) and the crystalline cone cells (C). Three retinular cells (R) were clearly visible, but six to eight have been reported in previous literature (Huvard 1990; Land and Nilsson 1990). A singe cone cell nucleus (C) was visible; the other may have been lost during preparation. Scale bar: (A, B) 500 μm, (C, D, F) 40 μm, (F) 55 μm (G, H, I) 15 μm. DAPI, 4',6-diamidino-2-phenylindole.
The surprising presence of eyes in male, but not female E. morini raises a number of questions. The first is, “Why?” In natural history, “why” questions are evolutionary questions. Why has a particular feature evolved to its present form? Evolutionary hypotheses are often inspired by adaptive explanations – what benefit does a particular trait bestow upon the individuals that posses it? Based on adaptive reasoning, and our knowledge of the natural history, we are currently testing two hypotheses to explain why E. morini males have eyes, but females do not.
The first idea is that males might be using their eyes to find mates. In nature, when females and males differ significantly, the reason often boils down to mating, to the process called sexual selection. Sexual selection occurs when sex-specific traits, like peacock feathers or larger body size, increase the chance of mating. If the trait is heritable, increased mating success will cause the trait to become more common. Peacocks with longer tail features are more attractive and may mate more often, having sons with longer tail feathers. In E. morini, males having eyes might allow them to find more mates.
A second explanation for differences between male and female E. morini is that differing life histories impose different demands on their visual systems. Specifically, we hypothesize that males encounter higher exposure to predators than females. In the E. morini and its closest ostracod relatives (the myodocopids), mating occurs in the water column. Even though most ostracods spend most of their lives in the sediment at the bottom, many swim toward the surface in search of romantic encounters, not unlike the nuptial flights of social insects like ants and bees, where virgin queens take flight to mate. It is at this time, during mating, that E. morini might be especially susceptible to predation, for example by fishes seeking a tasty crustacean morsel. Since females seem to mate only once, and males seem to enter the water column night after night to look for a mate, the males have a higher chance of becoming a meal. Perhaps their eyes allow them to avoid this fate. This predation risk hypothesis is based on piecing together information about myodocopid life history – how then do we know when these tiny animals mate, and how often they mate?
Although we currently know very little about the life history of Euphilomedes morini, we are making informed guesses based on related ostracod species. We perhaps know the most about a different family, the Cypridinidae, studied by James Morin (the namesake of E. morini) and Anne Cohen. Most cypridinid ostracods live in the warm waters of the Caribbean Sea. Since the animals produce a bright blue light (bioluminescence) that is visible by humans, and since the ostracods use this light as a pre-mating display, humans can study aspects of behaviors that could not be studied in E. morini, which does not produce light. Not unlike fireflies that are conspicuous on midsummer’s nights in the eastern and central US, the Caribbean cypridinids (‘sea fireflies’) produce coded messages by flashing. Male sea fireflies swim into the water column shortly after sunset and begin flashing their bioluminescent signal in hopes of attracting a female. Some males, called ‘sneakers’, follow the more industrious males without producing any light codes themselves. These sneakers hope to mate with an attracted female, without expending the energy to produce the signal. Mating presumably takes place in the water, after which females brood their young inside their shells. In captivity, females stored sperm from one mating event, which was used to fertilize multiple broods, and the females might not mate again after their first nuptial swim.
Fig 3. Small blue circles represent discrete flashes of light produced by male bioluminescent cypridinid ostracods. Patterns of different species are illustrated, with white arrows showing the direction of swimming of an individual animal producing the pattern over time. Each pattern is characteristic of a different species and are performed above different microhabitats. Original figure in black and white line drawing by Jim Morin and Anne Cohen. Color and photos added by T. Oakley.
There is also indirect evidence that Euphilomedes females only mate once and that males seek mates more often. In museum-preserved animals, females with broods are missing their swimming appendages. In many of these females, swimming appendages have been found in their guts. This suggests that after mating, female Euphilomedes consume their own swimming appendages, committing them to a celibate life in the sediment. Such behavior may seem strange by human standards, but it is not without analog in other animals. For example, ants hydrolyze their flight muscles after their nuptial flight, gaining energy from a structure that will no longer be needed. In contrast to females, we think that Euphilomedes males swim in search of females more commonly. In Puerto Rico, we found by sweeping nets through the water that swimming males outnumbered swimming females some 1000:1 at the peak activity time after sunset. Taken together, these data suggest a life history whereby eager males swim very often in search of mates. But females spend much less time swimming, instead mating once or few times before returning to the sediment to brood their young. All these small swimming male ostracods could provide a feast for predators such as small fishes, which are known to consume Euphilomedes.
To test the hypotheses that male E. morini eyes help them find mates and/or help them evade predators, we will make calculations of their optics, and perform behavioral experiments. Estimates of the visual abilities of males can be made by measuring aspects of their eyes, such as the number of facets, and the size of the lenses. If male eyes have enough resolution to see larger predators at a distance, but not enough resolution to see females until they are very, very close; this would support the predator-evasion hypothesis. We will also experimentally inhibit the vision of males. If the experimental animals are poorer at finding mates or evading predators, either hypothesis could be supported. Nature often shows us that there are multiple answers for “why” questions, perhaps even some answers we have not considered here.
For many, the beauty and allure of biology lies in the rich diversity of life. This diversity is apparent when we gaze at a tangled bank, or hike through a rainforest. But this amazing diversity is everywhere. The next time you walk on Stearn’s Wharf or Goleta Pier realize that many amazing creatures are living just meters below your feet. Even the cryptic have lessons to teach us about biodiversity.