Proc. Nat. Acad. Sci. USA Vol. 71, No. 9, pp. 3517-3521, September 1974 Three Flies and Three Islands: Parallel Evolution in Drosophila (Caribbean Sea/Indian Qcean/ecology/land crabs) HAMPTON L. CARSON Department of Genetics, University of Hawaii, Honolulu, Hawaii 96822 Communicated by Th. Dobzhansky, May 9, 1974 ABSTRACT Most organisms are evolutionary conserva- status of the species that he studies and decide which are the tives; they may subdivide their niches but tend to remain which promise of be- within them. Yet the fossil record shows many cases of unalterable "conservatives" and gives breakthrough to a new mode of life. How may such evolu- coming the rare "liberal" that starts in a new direction. tionary innovation be recognized at this time level? Three In many world-wide groups of organisms, the most unusual species of Drosophila have accomplished an innovation in and deviant members are found on islands. An island need not that they breed as obligate commensals on tropical land be literally defined; caves and isolated mountain peaks qualify crabs. This could be dismissed as a curious aberration were it not for the fact that the three flies concerned repre- in the present context (2). The peculiarities of island life are sent three different phyletic lines of the family. Although often dismissed as evolutionary cul-de-sacs, interesting only Drosophila is abundant on the continents, these three as oddities arising in an isolated and often discordant eco- parallel innovative evolutions have occurred on islands. system. In my view, these unusual evolutionary events de- The proposal is made that the genetic systems of many for the conservative groups of organisms carry variability that mand special attention as possible prototype systems would permit them to evolve in a novel direction. The evolutionary synthesis of novelties. realization of this capacity, however, is possible only under special environmental conditions. The biology of Drosophila New information that has come to light on certain members Evolutionary innovation of the family Drosophilidae may suggest ways to approach As they occur on the continents, the members of a family of the problem of evolutionary innovation. Probably more is organisms tend to be conservative in their adaptations. Once known about the comparative genetic systems of Drosophila a basic ecological niche has been conquered, evolution leading than any other closely knit group of higher organisms. Less in a drastically different direction is rare. Related species widely recognized is the fact that such genetic studies can tend to repeat the old theme with only minor variations. now be interpreted in the light of an increasingly sophisticated Thus, most contemporary species belonging to a single family knowledge of the systematics and ecology of these flies. Ap- have a certain dull sameness about their ecologies, even in proximately 2500 species of the family have been described, the presence of sprightly morphological differences. and data on the life histories of many species have accumu- Most differences between species do indeed have ecological lated. Most species are local endemics; only a few have come meaning, but this lies often in the development of delicate and to be associated with man on a world-wide basis (3, 4). recondite methods of packing species into an ever increasingly Drosophila are small, highly vagile insects that subsist on subdivided niche and avoiding competition. Although such microorganisms, especially yeast and bacteria. The common microadaptational developments are biologically important, substrates supporting the relevant microorganisms in nature they rarely provide clues as to how large-scale evolutionary are fruit, fungus, flowers, bark, roots, slime flux (infected sap innovations are accomplished. Yet, when confronted with the flows), fallen leaves, and broken stems. As decay begins, fossil record, one sees abundant evidence of biological break- Drosophila is usually one of the first insects to arrive. The throughs from one basic adaptive norm to another. adults feed both on the carbohydrates and proteins released Everyone knows, for example, the famous diagram showing from the substrates, and subsequently they consume the "adaptative radiation" in the mammals (1). A small terres- microorganisms themselves. Drosophila flies are usually trial generalist sits in the center of the picture, surrounded opportunistic as feeding adults; they visit many types of by a circle of representatives of the different families; there ephemeral carbohydrate sources before the latter dessicate. are burrowing, flying, aquatic, and arboreal forms. Surely Oviposition by gravid females tends to be much more precise, the characters that adapt these organisms, now so useful in and breeding sites are often visited by only one or a few the systematic diagnosis of higher-order differences, each species. must have had its inception in some real, ancient Mendelian population. Is our ingenuity, technical skill, and scientific Drosophila and land crabs imagination not great enough to decipher such beginnings? Departing drastically from the above pattern are three species Or are they so infrequent as to preclude their being recog- of drosophilid flies from insular areas; two of these are from nized at the present time level? Is the microevolutionist in- the Caribbean Sea and one is from the Indian Ocean. Each escapably condemned to remain mired in trivia? stems from a different phyletic line, yet each has evolved, What sort of change, at the present time level, might indeed in closely parallel fashion, into a truly novel ecological associa- constitute the microevolutionary inception of innovative tion for the family. They have adopted an intimate associa- evolution? Each ecological geneticist must survey the adaptive tion of obligate commensalism with land crabs. 3517 Downloaded by guest on October 1, 2021 35183518Zoology:Zoology:CarsonCarson~~~~~~~~~~~~Proc.Nat. Acad. Sci. USA 71 (1974) TABLE 1. Comparison of three species of crab Drosophila The decapod Crustacea are primarily aquatic animals. Nevertheless, within several families, groups of species have Drosophila Lissocephala evolved that have at least partially conquered terrestrial Drosophila endobranchia Powelli habitats, especially in the tropical parts of the world. Because carcinophila Carson and Carson and the adults live out much of their lives above the tide Wheeler Wheeler high Species Wheeler level, these animals are commonly referred to as land crabs, Subgenus Drosophila Sturtevant although all of them apparently retain aquatic larval stages. Species re,'pleta quinaria- Separate Crabs belonging to two genera of the family Gecarcinidae, group (mercatorum virilis section subfamily Gecarcinus and Gecarcoidea, are especially adapted for ter- complex) (aberrant restrial life; these two are the most important hosts for the form) obligatory Drosophila commensals. The two genera are Distribution Nreo'tropical Holarctic Africa, south1- closely similar and together include forms that have of group east Asia, global Micronesia pan-tropical oceanic distributions, being largely confined to Distribution Islands -of West Cayman' Christmas small, isolated, but richly vegetated islands. Descriptions of of species Indies and Islands and Island, these three cases of Drosophila commensalism have recently Caribbean Sea Cuba Indian Oc3ean been published (5, 6, 8). The three are compared and the (widespread) basic facts a-re summarized in Table 1. What follows is a brief Sympatry All three species allopatric account of the biological relationships observed as the three Group Cactus breeding Fungus and/ Fungus flies and their crabs have been studied on three islands. or bark ecology breeding? Drosophila carcinophila- on Cat Cay. North Cat Cay is a breeding? small Crab hosts Gecarcinus8 Gecarcinus Gecarcoidea island in the Bahamas south of the Bimini group, about km east ruricola ruricola; humei; Bii,rgus 80 of the Florida coast (northernmost closed circle, Gecarcinus latro; Geo- Fig. 1). Cat Cay is separated from neighboring Gun Cay by a lateralis grapsus crrini- strait, which is a'bout 400 m wide. Both islands are less than pes; Cardi- 3 km long and rise no more than, 10 mn above sea level. De- soma carnifex spite their narrowness (150-200 in), both support sub- Adult flies Have three pairs of dorsocentral Normal dorso- stantial broadleaf coppices growing on the rich black lime- bristles centrals stone soil. This is the habitat of Gecarcinus ruricola, a large Normal Posterior Normal semi-fossorial land crab. These crabs are especially abundant scutellars scutellars scutellars on Gun which is uninhabited a small turned Cay, except for light- up- G. ruricola rare or on right and house. is absent Bimini, and one may crossed conjecture that this is due primarily to the fact that the Size 2.5 mm 3.8 mm 2.0 mm crab is considered a culinary delicacy. It is, therefore, (length) relentlessly hunted down in the populated parts of its range. Feeding Wholly on host: rarely if ever Mostly off the Although it was apparently once common throughout the leave crab; will not come to host; come Greater and Lesser Antilles, it remains today principally on' baited traps readily to small, isolated islands. baits The Black Crab, as it is commonly known in the area, is a Egg 4 long filaments; 2 short fila- 12 short fila- strictly terrestrial 'animal, being largely confined to dense placement on ments; ce- ments; place- forest, where it excavates shallow burrows under limestone crab in un- mented on ment at base rocks or tree roots. Despite its common name, it shows exten- known site carapace, of 2nd anten- sive color polymorphim. The crabs apparently leave the near eyes na forests the brief when Larvae All instars re- First inistar in First and third onlyduring spawning season, they migrate as main in ex- nephric instars in to the hard coastal limestone, known the "iron shore." ternal nephric groove; 2nd nephric This is a spectacular mass migration, which occurs only once groove instar in groove; 2nd a year; the crabs remain at the shore briefly and then migrate branchial instar in back to the forests.