Stalk-eyed flies are insects of the fly family Diopsidae. The family is distinguished by the possession of eyestalks: projections from the sides of the head with the eyes at the end. Some fly species from other dipteran families such as the Drosophilidae and Tephritidae carry similar structures but the unique character of the Diopsidae is that the antennae are carried next to the eye at the end of the stalk.

Stalk-eyed flies have been subject to a considerable amount of research due to their unique morphology and how it has arisen through forces of sexual selection and natural selection. As such, the behavior of the stalk-eyed fly has given key insights into the development of sexual ornamentation, the genetic factors that maintain such morphological feature, sexual selection, and the handicap principle.

Taxonomy

Stalk-eyed flies are members of the family Diopsidae, first described by Dr. John Fothergill^[1] and named by Carl Linneaus in 1775.^[2] The family Diopsidae is contained within the order Diptera and suborder Cyclorrapha, and features some 150 described species. This small family of flies contains members with a specific and unique morphology, their eyes being borne on stalks.^[3]

An African genus Centrioncus once placed in the Sepsidae and then moved to the Diopsidae had been suggested as belonging to a proposed new family Centrioncidae as a sister group of the Diopsids^[4] but this is usually treated as a subfamily.^[5]

Species list

• Genus Centrioncus
  • Species Centrioncus aberrans
  • Species Centrioncus angusticercus
  • Species Centrioncus bytebieri
  • Species Centrioncus decellei
  • Species Centrioncus decoronotus
  • Species Centrioncus jacobae
  • Species Centrioncus prodiopsis

• Genus Cladodiopsis
  • Species Cladodiopsis leptophylla
  • Species Cladodiopsis seyrigi
  • Species Cladodiopsis sicardi

• Genus Diasemopsis
  • Species Diasemopsis aethiopica
  • Species Diasemopsis albifacies
  • Species Diasemopsis amora
  • Species Diasemopsis apicifasciata
  • Species Diasemopsis comoroensis
  • Species Diasemopsis concolor
  • Species Diasemopsis coniortodes
  • Species Diasemopsis conjuncta
  • Species Diasemopsis dejecta
  • Species Diasemopsis disconcerta
  • Species Diasemopsis dubia
  • Species Diasemopsis elegantula
  • Species Diasemopsis elongata
  • Species Diasemopsis exquisita
  • Species Diasemopsis fasciata
  • Species Diasemopsis fusca
  • Species Diasemopsis fuscapicis
  • Species Diasemopsis fuscivenis
  • Species Diasemopsis hirsuta
  • Species Diasemopsis hirta
  • Species Diasemopsis horni
  • Species Diasemopsis incerta
  • Species Diasemopsis interrupta
  • Species Diasemopsis jeanneli
  • Species Diasemopsis jillyi
  • Species Diasemopsis latifascia
  • Species Diasemopsis longipedunculata
  • Species Diasemopsis meigenii
  • Species Diasemopsis minuta
  • Species Diasemopsis munroi
  • Species Diasemopsis nebulosa
  • Species Diasemopsis obscura
  • Species Diasemopsis obstans
  • Species Diasemopsis pleuritica
  • Species Diasemopsis pulchella
  • Species Diasemopsis quadrata
  • Species Diasemopsis robusta
  • Species Diasemopsis sexnotata
  • Species Diasemopsis siderata
  • Species Diasemopsis signata
  • Species Diasemopsis silvatica
  • Species Diasemopsis subfuscata
  • Species Diasemopsis thaxteri
  • Species Diasemopsis thomyris
  • Species Diasemopsis wolteri

• Genus Diopsina
  • Species Diopsina draconigena
  • Species Diopsina ferruginea
  • Species Diopsina intermedia
  • Species Diopsina kwaipai
  • Species Diopsina nitida
  • Species Diopsina schulteni

• Genus Diopsis'
  • Species Diopsis abdominalis
  • Species Diopsis absens'
  • Species Diopsis acanthophthalma
  • Species Diopsis angustifemur
  • Species Diopsis anthracina
  • Species Diopsis apicalis
  • Species Diopsis arabica
  • Species Diopsis aries
  • Species Diopsis atricapilla
  • Species Diopsis atromicans
  • Species Diopsis baigumensis
  • Species Diopsis basalis
  • Species Diopsis circularis
  • Species Diopsis collaris
  • Species Diopsis confusa
  • Species Diopsis cruciata
  • Species Diopsis curva
  • Species Diopsis dimidiata
  • Species Diopsis diversipes
  • Species Diopsis eisentrauti
  • Species Diopsis erythrocephala
  • Species Diopsis finitima
  • Species Diopsis flavoscutellaris
  • Species Diopsis fumipennis
  • Species Diopsis furcata
  • Species Diopsis globosa
  • Species Diopsis gnu
  • Species Diopsis hoplophora
  • Species Diopsis ichneumonea
  • Species Diopsis indica
  • Species Diopsis leucochira
  • Species Diopsis lindneri
  • Species Diopsis macquartii
  • Species Diopsis macromacula
  • Species Diopsis macrophthalma
  • Species Diopsis maculithorax
  • Species Diopsis melania
  • Species Diopsis micronotata
  • Species Diopsis munroi
  • Species Diopsis neesii
  • Species Diopsis nigra
  • Species Diopsis nigrasplendens
  • Species Diopsis nigriceps
  • Species Diopsis nigrosicus
  • Species Diopsis nitela
  • Species Diopsis orizae
  • Species Diopsis ornata
  • Species Diopsis phlogodes
  • Species Diopsis planidorsum
  • Species Diopsis pollinosa
  • Species Diopsis preapicalis
  • Species Diopsis punctigera
  • Species Diopsis rubriceps
  • Species Diopsis servillei
  • Species Diopsis somaliensis
  • Species Diopsis subfasciata
  • Species Diopsis sulcifrons
  • Species Diopsis surcoufi
  • Species Diopsis terminata
  • Species Diopsis trentepohlii
  • Species Diopsis wiedemanni

• Genus Eurydiopsis
  • Species Eurydiopsis brevispinus
  • Species Eurydiopsis glabrostylus
  • Species Eurydiopsis helsdingeni
  • Species Eurydiopsis pachya
  • Species Eurydiopsis porphyria
  • Species Eurydiopsis pseudohelsdingeni
  • Species Eurydiopsis sarawakensis
  • Species Eurydiopsis subnotata

• Genus Pseudodiopsis
  • Species Pseudodiopsis bipunctipennis
  • Species Pseudodiopsis detrahens

• Genus Sphyracephala
  • Species Sphyracephala beccarii
  • Species Sphyracephala brevicornis
  • Species Sphyracephala europaea
  • Species Sphyracephala hearseiana
  • Species Sphyracephala munroi
  • Species Sphyracephala subbifasciata

• Genus Teleopsis
  • Species Teleopsis adjacens
  • Species Teleopsis africana
  • Species Teleopsis anjahanaribei
  • Species Teleopsis apographica
  • Species Teleopsis apollo
  • Species Teleopsis boettcheri
  • Species Teleopsis currani
  • Species Teleopsis dalmanni
  • Species Teleopsis discrepans
  • Species Teleopsis fallax
  • Species Teleopsis ferruginea
  • Species Teleopsis fulviventris
  • Species Teleopsis krombeini
  • Species Teleopsis maculata
  • Species Teleopsis motatrix
  • Species Teleopsis onopyxus
  • Species Teleopsis orientalis
  • Species Teleopsis pharao
  • Species Teleopsis quadriguttata
  • Species Teleopsis quinqueguttata
  • Species Teleopsis rubicunda
  • Species Teleopsis selecta
  • Species Teleopsis sexguttata
  • Species Teleopsis shillitoi
  • Species Teleopsis sinensis
  • Species Teleopsis sykesii
  • Species Teleopsis thaii
  • Species Teleopsis trichophoras
  • Species Teleopsis vadoni
  • Species Teleopsis whitei

• Genus [[Teloglabrus
  • Species Teloglabrus australis
  • Species Teloglabrus curvipes
  • Species Teloglabrus duplospinosus
  • Species Teloglabrus entabensis
  • Species Teloglabrus lebombensis
  • Species Teloglabrus londti
  • Species Teloglabrus milleri
  • Species Teloglabrus pelecyformis
  • Species Teloglabrus prolongatus
  • Species Teloglabrus sabiensis
  • Species Teloglabrus sanorum
  • Species Teloglabrus stuckenbergi
  • Species Teloglabrus trituberculatus
  • Species Teloglabrus tsitsikamensis
  • Species Teloglabrus vumbensis

Distribution and habitat

There are several hundred species in the family, with the greatest diversity found in the Old World tropics.^[6] They are distributed throughout the region, with the best known species being from South-East Asia and Southern Africa. There are also two species in North America and a European species has recently been found in Hungary.^[7]

Adult diopsids are typically found on low-lying vegetation in humid areas, often near streams and rivers, where they feed on fungi and bacteria on decaying vegetation. The larvae develop in rotting vegetation. Due to their peculiar morphology, stalk-eyed flies are readily identifiable as fossils (e.g. in amber); one such prehistoric genus is Prosphyrocephala.^[8]

Morphology

Stalk-eyed flies are small to medium-sized flies, ranging from about 4.0 to about 12.0 millimeters in length. Their heads are subtriangular, with variably produced transverse eye stalks in all genera except the African genus Centrioncus. The head is usually sparsely haired, with vibrissae (whiskers) absent.^[9]

The posterior (anatomy) portion of the fly's metathorax, or scutellum (insect), has a pair of stout processes, and often the laterotergite (one of a number of lateral flanges) of the postnotum (a small dorsal sclerite on the insect thorax posterior to the notum) has a dome-like swelling or spine-like process. The anterior femora of the legs are stout, with ventral spines. The larvae are saprophagic or phytophagous, eating decaying and fresh plant matter. Adult males have lost tergites seven and eight, and the seventh sternite forms a complete ventral band. ^[9]

Stalk-eyed flies possess eyestalks. Their eyes are mounted on projections from the sides of the head near the antennae. A rather remarkable feature of stalk-eyed flies is the ability of the males, shortly after they emerge from their pupae, to ingest air through their oral cavity and pump it through ducts in the head to the tips of the eye stalks, thereby elongating them while they are still soft and transparent.^[10]

Behavior

Vision

Despite the unusual morphology of the eye, each compound eye sees a region of space extending over more than a hemisphere in all directions. Thus, there is extensive binocular overlap, with about 70% of the ommatidia of each eye having a binocular partner ommatidia in the opposite eye which views in the same direction.^[11][12] The binocular field is most extensive in the frontoventral quadrant, where it reaches over 135 °, and is smallest in the dorsal region. Researchers found that the behavior of stalk-eyed flies is very much determined by vision. During the day, temporary territories may be defended by threatening behavior. At dusk the animals gather in small groups on selected threadlike structures, returning to the same site each day. When males of about equal size encounter one another within such a group they may engage in ritualized fights (or occasionally contact fights). Competitors are driven away by the dominant male. Conspecifics are most likely to elicit a threat or flight reaction when they are at a distance of about 50 millimeters, and reactions to model flies and reflections in a mirror also occur at about this distance.^[11]

Mating

Male Teleopsis dalmanni

Stalk-eyed flies roost at night on root hairs hanging by streams. Mating usually takes place in the early morning in the vicinity of their roosts. Females show a strong preference for roosting and mating with males with longer eyestalks, and males compete with each other to control lekking aggregations through ritualized contest. This contest involves males facing one another and comparing their relative eye spans, often with the front legs spread apart, possibly to emphasize their eye-stalk lengths .^[13] Male stalk-eyed flies with long eyestalks gain mating advantages both because of female choice and because of they are better able to compete with rival males.^[6][14]

Sexual selection

Though the evolution of exaggerated male traits due to female mate choice was at one point considered rather controversial, stalk-eyed flies are now regarded as a classic example of animals that exhibit sexually selected traits.^[15][16][17] One view maintains that male ornaments co-evolve with female preferences. The selection of an ornamented mate causes genes that influence expression of the selected male trait and genes coding for female preference for this trait to be passed on to offspring ^[18][19] This process creates linkage disequilibrium between selected alleles, with the magnitude of resulting genetic correlations influencing evolutionary outcomes. If the genetic correlation is high relative to the heritability of the male ornament, then a runaway process can occur leading to extreme sexually selected traits, such as the incredible eye spans observed in male stalk-eyed flies. Otherwise, the trait and preference for the trait increase until viability natural selection against further trait elaboration balances sexual selection.^[18]

Close up of a male Teleopsis dalmanni

The extreme morphology exhibited by the stalk-eyed fly (especially males) has been studied in an effort to support the hypothesis that exaggerated male traits could evolve through female mate choice and that the selection on male ornaments should cause a correlated response in female preferences. Researchers noted that the flies roosted along stream banks in peninsular Malaysia and that the males with the largest eye spans were accompanied by more females than males with shorter eye spans. From January to October, the researchers counted males and females on 40 root hairs along a single 200 meter stretch of stream bank in order to confirm this observation.^[20]

Sexual selection experiments

Researchers then collected stalk-eyed flies and observed their behavior under laboratory conditions. In the lab, each individual was scored for eye spans, body length, age and fecundity.^[21] Four experiments using pairs of males differing in eye span but matched in body length were conducted to quantify mate choice in the presence and absence of male interactions. Test males were created by artificial selection in which 10 of 50 males with the longest or shortest eye span to body length ratios were mated with 25 randomly chosen females. In each experiment, sets of five females were placed in clear, vented cages with selected line males. Wilkinson and Reillo then tested female choice in the presence and absence of male competition and in the presence of males with abnormally long and abnormally short eye spans.^[20]

It was found that males dispersed themselves while females clustered in certain areas of the cage. As observed prior to the study, researchers found that the average number of females per male increased with male eye span in field collected aggregations of stalk-eyed flies. Under laboratory conditions, researchers found that female preferences for male characteristics changed as the males sexual characteristics changed. After 13 generations of artificial selection, they found that long eye span male line females (i.e. females whose fathers had long eye spans) preferred long eye spans in both the selected males and in males that were not bred through artificial selection, while short eye span male line females (i.e. females whose fathers had short eye spans) found short eye spans to be the most attractive, even over males with long eye spans. Because researchers kept the females separate from males prior to mate selection, the change in female mate choice was genetically based and not learned. Thus, stalk-eyed flies have been able to evolve sexual trait in males that corresponds directly traits that affect mating choices made by females.^[20]

Stalk-eyed fly (Diasemopsis) (4561140578)

Handicap selection

However, the evolution of extreme morphology in male flies and the corresponding evolution of female preference toward these characteristics due to sexual selection is only half the picture.^[22] Handicap models of sexual selection (see Handicap Principle) predict that male sexual ornaments have strong condition-dependent expression and this allows females to evaluate male genetic quality.^{[23][24][25][26][27]}

Researchers have demonstrated that genetic variation underlies the response to environmental stress, such as variable food quality, of male sexual ornaments, such as the increased eye span, in the stalk-eyed fly.^[22] Researchers showed that some male genotypes develop large eye spans under all conditions, whereas other genotypes progressively reduce eye spans as environmental conditions deteriorate. Several non-sexual traits, including female eye span and male and female wing length, also show condition-dependent expression, but their genetic response is entirely explained by scaling with body size. Unlike these characteristics, male eye span still reveals genetic variation in response to environmental stress after accounting for differences in body size. Thus, it could be inferred that these results strongly support the conclusion that female mate choice yields genetic benefits for offspring as eye span acts as a truthful indicator of male fitness. Eye span is therefore not only selected on the basis of attractiveness, but also because it demonstrates good genes in mates.^[22]

Furthermore, it has been demonstrated that some populations of stalk-eyed fly female carry a meiotic drive gene on their X-chromosomes that causes female-biased sex ratios.^[28] In these populations, males which carry a gene to suppresses X chromosome meiotic drive have longer eyestalks. Thus, females that mate with these males gain a direct genetic benefit by producing male offspring in a female-biased population. In other words, the gene for long eye-stalks is linked to a gene that makes males to sire more male offspring.^[29] Alternatively, long stalks may signal fertility, perhaps by encouraging females to use the sperm of a long-stalked male so as to produce more fertile sons.^[29]

References