Hume, J. P. . The history of the dodo Raphus cucullatus and the penguin based largely upon sexually dimorphic characters pos- of Mauritius. Historical Biology : –. sessed by males and thought to be used mainly in court- Hume, J. P., and A. S. Cheke. . The white dodo of Réunion Island: unravelling a scientifi c and historical myth. Archives of Natural History ship and mating. These characters range from elaborately : –. pigmented wings to elongate setae, cilia, and bristles Moree, P. . A concise history of Dutch Mauritius, 1598–1710. on the forelegs to unique structures on the mouthparts London: Kegan Paul International. Mourer-Chauviré, C., R. Bour., S. Ribes., and F. Moutou. . The avi- and forelegs (Fig. ). The wide variety of secondary sex- fauna of Réunion Island (Mascarene Islands) at the time of the arrival of ual characters possessed by males of the various species the fi rst Europeans. Smithsonian Contributions to Paleobiology : –. groups suggests that sexual selection may have played an Owen, R. . Memoir of the dodo (Didus ineptus, Linn.). London: Taylor and Francis. important role in the diversifi cation of this group. Strickland, H. E., and A. G. Melville. . The dodo and its kindred. Approximately % of Hawaiian Drosophila are single- London: Reeve, Benham & Reeve. island endemics, possibly owing to their relatively poor fl ight abilities and low tolerance for desiccation. These physiological constraints, coupled with the unique geo- logical history of the Hawaiian Islands, have led to a spa- tially distributed pattern of diversifi cation referred to as DROSOPHILA the progression rule, where older species are found on older islands, and younger species are found on younger PATRICK M. O’GRADY, KARL N. MAGNACCA, islands (Fig. ). AND RICHARD T. LAPOINT One explanation for the large numbers of drosophi- lid species in the Hawaiian Islands involves adaptation University of California, Berkeley to so-called empty niches. This atmosphere of reduced competition allowed these species to experiment with The genus Drosophila provides excellent opportunities to novel life history strategies, and thus to diversify. Several study evolution on island systems. The endemic Hawaiian adaptations unique to the Hawaiian Drosophilidae seem Drosophila are a classic example of adaptive radiation and to bear this out. For example, the small group of ∼ spe- rapid speciation in nature evolving in situ over the course cies placed in the Scaptomyza subgenus Titanochaeta of the past million years. Other groups of Drosophila, have specialized to oviposit in spider egg sacs. Larvae found on true islands or in island-like systems (e.g., the develop and parasitize the spider eggs while they are Madrean Archipelago), are invaluable tools to under- being guarded by adult spiders. Sixty-seven percent of standing evolutionary biology and have served as theo- Hawaiian Drosophila for which data is available breed retical and empirical model systems for over years. on only a single host plant family, whereas % are spe- cifi c to a single host substrate, such as leaves, bark, or HAWAIIAN DROSOPHILA sap fl ux (Magnacca et al., ). The endemic Hawaiian Drosophilidae, with an esti- Hawaiian Drosophila have served as a model sys- mated species, consists of two major lineages, the tem to address a number of evolutionary phenomena, Hawaiian Drosophila and the genus Scaptomyza. The high including how founder events and mating asymmetries degree of species diversity in Hawai‘i is extraordinary, can drive species formation (Fig. ). Throughout their with about one-sixth of the world’s known Drosophili- evolutionary history, Hawaiian Drosophila have repeat- dae being endemic to this small archipelago. Phylogenetic edly undergone founder events, either as they colonize analyses indicate that the family colonized the Hawai- new islands or when populations are subdivided (e.g., ian Islands only once, roughly million years ago. The by lava fl ows or erosional processes). Hampton Carson genus Scaptomyza, which also contains a large number of utilized Hawaiian Drosophila to illustrate his founder mainland taxa, seems to have escaped from Hawai‘i and fl ush theory, a type of founder effect speciation that undergone subsequent diversifi cation on the mainland proposes a reduction in intraspecifi c competition and (see below). an increase in population size following a colonizing There are currently described species of Hawaiian event. Once the population size becomes large again, Drosophila, with an additional ∼ awaiting description. selection is reasserted, and the population may consti- These species have been divided into eight species groups tute a new species (Fig. ). (picture wing, nudidrosophila, ateledrosophila, antopocerus, Alan Templeton also used Hawaiian Drosophila to modifi ed tarsus, modifi ed mouthpart, haleakalae, rustica) explain his transilience founder effect theory. Templeton
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Gillespie08_D.indd 232 4/9/09 1:07:42 PM Kaneshiro extended founder effect theories to include the complex mating behaviors and secondary sexual char- acteristics exhibited by Hawaiian Drosophila. In most populations, females are very choosy in selecting males with which to mate. However, small, colonizing popula- tions are initially subject to founder effects, in which the scarcity of males forces females to be less selective when choosing a mate: If they are too choosy, they will not fi nd a mate. Additionally, males from this small popula- tion display highly variable mating behaviors because of reduced intraspecifi c competition and relaxed selection in what are normally highly selected behaviors (Fig. ). Choosy females from the larger source population will not mate with the males of the founder population, although females of this founder population will accept males from the larger source population.
CARIBBEAN DROSOPHILA Patterns of in situ species formation are not as clear in the Caribbean islands because many widely distributed spe- cies are also found in mainland North and South Amer- ica. Historically, this has led to a situation in which gene fl ow from closely related mainland populations can act to homogenize any unique genetic differences that may accu- mulate in island populations. In spite of the close prox- imity of mainland ancestors, some Caribbean Drosophila have become genetically distinct from these widespread ancestral species. The repleta and cardini groups highlight two factors, ecological specialization and morphological adaptation, that may act to drive the formation of new species in the presence of gene fl ow from the mainland.
FIGURE 1 Phylogenetic and morphological diversity in the Hawaiian Drosophilidae. Phylogeographic patterns in the planitibia species group of Hawaiian Drosophila showing four independent examples of the pro- gression rule in the cyrtoloma (blue), neopicta (green), planitibia (red), and picticornis (yellow) subgroups. Secondary sexual modifi cations on the forelegs of (A) D. waddingtoni and (B) D. quasiexpansa; the arista of (C) D. tanythrix; mouthparts of (D) D. xenophaga, (E) D. hystricosa, (F) D. adventitia, and (G) D. freycinetae; and the wing of D. grimshawi.
discussed how, after a bottleneck derived from a founder event, a highly outbred colonizing population would expe- rience a shuffl ing between epistatic loci that were adapted to work best in certain combinations (Fig. ). This would cause an instant shift in adaptive peaks to ones optimal for these randomly recombined loci. Although he con- cludes that this is likely a rare event, the ecological and
genetic nature of the Hawaiian Drosophila lend them to FIGURE 2 Comparison of founder fl ush, genetic transillience, and this sort of speciation. asymmetrical mating hypotheses.
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Gillespie08_D.indd 233 4/9/09 1:07:42 PM Ecological adaptation may be an important component SCAPTOMYZA AND ISLAND COLONIZATION of species formation. The Drosophila repleta group con- The cosmopolitan genus Scaptomyza (Diptera: Droso- tains about described species, the majority of which are philidae), with nearly described species placed in endemic to the New World and have diversifi ed on various subgenera constitutes a major radiation within the species of necrotic cacti. One group, the mayaguana triad, family Drosophilidae. About described species are is restricted to the Caribbean and includes the widespread endemic to Hawai‘i, and an additional ∼ from this species D. mayaguana, and the more narrowly restricted archipelago await description. Phylogenetic analyses taxa D. straubae and D. parisiena. Although few morpho- strongly support the monophyly of Scaptomyza and its logical differences distinguish these species, they do have placement as the sister group to the endemic Hawaiian unique polytene chromosome inversions and ecological Drosophila. Unlike the Hawaiian Drosophila, however, associations (different host cacti) that may have acted as a Scaptomyza males generally lack secondary sexual char- reproductive barrier to generate distinct species. acteristics and do not perform elaborate courtship dis- Caribbean island Drosophila have also been used as plays. Instead, they have complex genitalia that can be models to understand morphological variation and phe- quite different, even between closely related taxa, and notypic plasticity. The Drosophila cardini group consists may act to reinforce a “lock and key” form of species of neotropical species in two subgroups, cardini and recognition. dunni. The dunni subgroup is entirely Caribbean in dis- Biogeographic analyses suggest that the genus tribution; each species is endemic to a specifi c island in Scaptomyza originated in the Hawaiian Archipelago and the Greater and Lesser Antilles. These species display a has subsequently “escaped” from the islands and diversi- cline of abdominal pigmentation, with more lightly pig- fi ed on the continent. This is a particularly interesting mented species being found in the northwest, and darker biogeographic pattern, because no other known group species in the southeast (Fig. ). This pattern may be due of organisms has colonized a continent from Hawai‘i. to island endemics being more geographically isolated The genus Scaptomyza, perhaps because of its history of and having smaller population sizes, which can cause radiation on and migration from Hawai‘i, is extremely traits (e.g., color patterns) to become rapidly fi xed in the successful as a colonist of remote island archipelagos. population. However, studies on the genetic basis of this Of the currently recognized subgenera, over half pos- color variation suggest that genetic control of abdominal sess successful island radiations: Seven (Alloscaptomyza, pigmentation is highly malleable, with similarities in col- Elmomyza, Engiscaptomyza, Exalloscaptomyza, Grimsha- oration not necessarily refl ecting relatedness. womyia, Tantalia, Titanochaeta) are endemic to Hawai‘i, two (Bunostoma, Rosenwaldia) are known from the Pacifi c including Hawai‘i, one (Boninoscaptomyza) is endemic to the Ogasawara Islands south of Japan, and three (Lauxan- omyza, Macroscaptomyza, Trogloscaptomyza) are endemic to the South Atlantic islands of St. Helena and Tristan da Cunha. The South Atlantic islands Tristan da Cunha and St. Helena also host representatives of two wide- spread subgenera, Scaptomyza ( spp.) and Parascaptomyza ( spp.), for a total of eight endemic species. Other species in the subgenus Parascaptomyza are island endemics from such disjunct islands as the Azores, Canaries, Marquesas, Cape Verde, and Java. Many insect species lose the ability to fl y when they become fully adapted to island life. One species of brachypterous Scaptomyza, S. altissima, is known from Tristan da Cunha and Gough Islands in the South Atlantic. Outside of this example, the loss of fl ight in this family is rare, although the endemic Hawaiian Dro-
FIGURE 3 Spatial distribution of species and abdominal pigmentation sophila are signifi cantly less mobile than their mainland patterns in the Drosophila cardini group. counterparts.
234 DROSOPHILA
Gillespie08_D.indd 234 4/9/09 1:07:44 PM ISLAND-LIKE SYSTEMS enous and food wastes, respectively. The nephric groove The Madrean Archipelago is a system of mountain islands and its associated green gland host a unique assemblage of distributed across the southwestern United States and microorganisms that are suffi cient to support the complete northern Mexico. During the middle Pliocene, this area development of D. carcinophila and at least one instar of D. was characterized by a mild, warm, semiarid climate. Rapid endobranchia and L. powelli. Adaptation to this lifestyle from desertifi cation as a result of the uplift of the Sierra Nevada either a cactus or fungal ancestor most likely involves a suite and the coincident elevation in temperature over the past of changes in oviposition preference, olfactory and gustatory ∼. million years have led to the break-up of these plant receptors, and larval behavior. Recent genome sequencing and animal communities and their restriction to higher has facilitated the understanding the genetics of host-plant elevations. Present-day mountaintops in this region are association in the genus Drosophila, and similar studies will characterized by cooler, more mesic habitats than are the shed light on this fascinating ecological adaptation. surrounding arid deserts. Several groups of mycophagous SEE ALSO THE FOLLOWING ARTICLES species in the macroptera, rubrifrons, quinaria, and testa- cea species groups have formed in association with these Flightlessness / Founder Effect / Hawaiian Islands, Biology / Insect Radiations / Sexual Selection island systems because of their dependence on the fungi
that are geographically restricted to these areas. FURTHER READING In Drosophila innubila, paleoclimatic data suggest that Brisson, J. A., A. Wilder, and H. Hollocher. . Phylogenetic analysis populations may have been panmictic until , years of the cardini group of Drosophila with respect to changes in pigmenta- ago, when they became fractured into their present-day tion. Evolution : –. distributions. Signifi cant genetic differentiation between Carson, H. L. . The population fl ush and its genetic consequences, populations suggests that gene fl ow is restricted among in: Population biology and evolution. R. C. Lewontin, ed. New York: Syracuse University Press, –. these sky islands, and the high geographic variation in Carson, H. L., and A. R. Templeton. . Genetic revolutions in relation mitochondrial DNA may be due to an association with to speciation phenomena: the founding of new populations. Annual the male-killing Wolbachia endosymbiont, which tends to Review of Ecology and Systematics : –. Craddock, E. M. . Speciation processes in the adaptive radiation of accentuate the effects of genetic drift. Hawaiian plants and animals. Evolutionary Biology : –. Kaneshiro, K. Y., and C. R. B. Boake. . Sexual selection and speciation: PARALLEL EVOLUTION issues raised by Hawaiian Drosophila. Trends in Ecology and Evolution : IN ISLAND DROSOPHILA –. Magnacca, K. N., D. Foote, and P. M. O’Grady. Breeding ecology of the Island endemic species often evolve unique morphologi- endemic Hawaiian Drosophilidae. Zootaxa in press. cal structures, behaviors, or ecological associations. Some Markow, T., and P. M. O’Grady. . Evolutionary genetics of repro- adaptations may generate large radiations, such as the ductive behavior in Drosophila: connecting the dots. Annual Review of Genetics : –. Hawaiian Drosophila, whereas others, like the spider preda- O’Grady, P. M. . Species to genera: phylogenetic inference in the tors in Scaptomyza (Titanochaeta), are represented by only a Hawaiian Drosophilidae, in Molecular systematics and evolution: the- few species. An association between drosophilids and land ory and practice. R. DeSalle, G. Giribet, and W. Wheeler, eds. Berlin: Birkhauser Verlag, –. crabs, one of the most interesting ecological adaptations in this family, has occurred independently on three dif- ferent island systems. Although the majority of species in the repleta group are cactophilic, the West Indies endemic D. carcinophila has been reared from the crab species Gecar- DWARFISM cinus ruricola. Likewise, although the entire quinaria group is mycophagous, one representative, D. endobranchia, has SHAI MEIRI also been recorded from G. ruricola in the Cayman Islands Imperial College London, United Kingdom and Cuba. Similarly, within the predominantly mycopha- PASQUALE RAIA gous Lissocephala, L. powelli from Christmas Island has been University of Naples, Italy recorded from several crab genera, including Gecarcoidea, Birgus, Geograpsus, and Cardisoma. All three crab fl y species have independently evolved the ability to utilize the exter- Insular dwarfi sm is a tendency of many island animals nal nephric groove or branchial chamber of these land crabs. to evolve a smaller size than their ancestors on the near These structures are involved in the excretion of nitrog- mainland. Dwarfi sm may be relatively minor but can
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