Mimicry is rife not just among animals, but among plants. But one group that’s been neglected in such studies is the juvenile stages of marine organisms. (This isn’t the case for juveniles of terrestrial animals, as seen by the numerous studies of caterpillar mimicry.)
This has begun to be remedied by a brand new study by Adam Greer and his colleagues published in Marine Ecology Progress Series (free pdf here). The authors give pretty convincing evidence that the larval stages of many fish have evolved to resemble either invertebrate zooplankton that are unpalatable or dangerous (larvae of tunicates and ctenophores), or don’t offer much of a food reward (the larvae of crustaceans). The mimicry, which involves shapes, ornamentation, and behavior of the larval fish, would be a form of Batesian mimicry, in which an edible species (the larval fish) comes to resemble either a distasteful, dangerous, or nutritionally worthless prey item (crustaceans and some invertebrates), because this kind of resemblance reduces your chance of being eaten. That, of course, is mediated by fish predators, who learn to avoid the worthless or dangerous prey and thereby select for larval fish to resemble those prey. It is a phenomenon that requires a learning predator.
Here are two examples of the “models” (“salps” are free-swimming larval tunicates) and putative mimics (larval fish), taken from the paper:
Here’s a figure with photographs, and I’ve put the caption below the figure. All the models on the left are invertebrates, and all the mimics on the right are larval fish. The authors note the various features of fish that presumably have been molded by natural selection to resemble the models: elongated body shape, stalked eyes, long fin rays, guts that trail behind the animal, and so on. The paper notes the various traits of fish that have evolved to look like invertebrates:
The resemblances of different larval fishes to members of the gelatinous zooplankton community are striking when viewing general body shape, transparency, and positioning of fin rays. Gelatinous zooplankton often have long, delicate tentacles that can be readily observed using in situ imaging. These tentacles typically contain pigmented or translucent ‘notches’ that are budding cormidia or nematocysts in siphonophores and hydromedusae or, in ctenophores, branches that increase cross-sectional area and improve prey capture ability. Many larval fishes have evolved delicate and elaborate fin ray extensions that closely resemble the tentacles of siphonophores and ctenophores, including small swellings that resemble the ‘notches’ (Fig. 1A−D). In the Liopropoma genus of groupers, these long fin rays have been taken to an extreme, with 2 rays extending sev- eral times the body length (Fig. 1D). The general shape and positioning of the dorsal fin ray on many flatfishes resemble salps and the projection of their tunics (Fig. 1E,F). The closest resemblance between fish larvae and gelatinous zooplankton is seen in the leptocephalus larvae that are almost identical to a cestid ctenophore (Fig. 1G,H).
Fig. 1. Example images of morphological and behavioral mimicry showing less palatable models (from the perspective of a vi- sual predator) and corresponding mimics in their natural orientation: (A) ctenophore Euplokamis dunlapae; (B) calycophoran siphonophore; (C) flatfish larvae (Paralichthyidae), note pigmented swellings similar to A and B; (D) grouper larva (Liopropoma spp.), note pigmented swellings similar to A and B; (E) salp (Thalia spp.); (F) flatfish larva (Bothidae); (G) cestid ctenophore; (H) leptocephalus eel larva (Muraenidae); (I) leptocephalus larva in curled posture with similar appearance to a salp; (J) narcomedusa Solmundella bitentaculata; (K) flatfish larvae in curled posture; (L) chaetognath (Sagitta spp.); (M) anchovy larva (Engraulidae); and (N) clupeid larva (Clupeidae) vertically orienting. Note changes in scale bars among images
The extensions and ornaments that make the fish resemble the larvae are thought to be costly, because they reduce swimming ability. But if the fitness loss due to slower swimming is more than offset by the survival advantage of resembling an animal that predators avoid, then the mimicry will evolve.
The authors also note that some of the mimicry, as it often does, involves behavior: larval fish that are mimics like these tend to float around like their models, with their bodies curled, something that nonmimetic larval fish don’t do.
Now the evolution of mimicry is inferred, but there’s pretty good evidence for it. First of all, the larval fish are located in the same areas as the models, generally (but not always) a requirement for Batesian mimicry to evolve (predators must apply their learned avoidance to fish evolving mimicry). In this case, the models and mimics were trawled from the ocean in the Gulf of Mexico as well as off New England in the U.S. Second, predation by fish has led to other cases of mimicry (camouflage) in adult rather than juvenile fish, so the selective pressure—fish predation—is present. Further, there is high abundance of the invertebrate zooplankton in the place where mimetic fish larvae live, and a high density of models is usually thought to be necessary in most cases of Batesian mimicry (predators must encounter the model fairly frequently, so that their aversion is reinforced compared to when they encounter the tasty mimic, which reduces aversion).
As I said, the mimicry hypothesis is intriguing but tentative. One experiment that could be done, but hasn’t been, is to expose predatory fish in the laboratory to some of the nutritious models as well as to palatable prey, let them learn to avoid the former, and then test the schooled fish (pardon the pun) by putting them with mimetic larval fish. If this is truly mimicry, predators will then avoid the larval fish mimics a lot more than they would avoid non-mimetic larval fish. In control experiments in which fish haven’t learned, they should nom up the mimetic fish larvae.
Finally, the authors do a computer simulation to show that even a tiny selective advantage of fish larvae, making them more closely resemble the models, will lead to a rapid evolution of mimicry. (We already knew this from early work on population genetics, but it’s useful to reprise.) Since larval fish are produced in huge numbers, with the vast majority dying before reproduction, the authors assumed a mortality of 0.999999 among 1 million larvae released. They they added two traits, a behavioral one and a morphological one, that reduced the mortality slightly—to 0.9999937 when both traits were present. Running this simulation over only 5000 generations showed a rapid increase in the frequency of both traits. (We used computer simulations like this one in my evolution course: you just plug in the survival values and generation numbers, and get a printout of the results.) 5000 generations, of course, is just an eyeblink in evolutionary time.
While the evidence for Batesian mimicry in larval fishes isn’t absolutely conclusive, it’s pretty strong based on the strong resemblance—involving both morphology and behavior—and the fact that the models are, according to the authors, avoided by predators. A few laboratory experiments like those I suggest above would make the argument nearly watertight—excuse the second pun.
Greer, A. T., C. B. Woodson, C. M. Guigand, and R. K. Cowen. 2016. Larval fishes utilize Batesian mimicy as a survival strategy in the plankton. Marine Ecology Progress Series 551:1-12.