Stalk-eyed fly

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Stalk-eyed flies
Temporal range: Eocene–Recent
Diopsid2.jpg
A diopsid from Cameroon
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Diptera
(unranked): Cyclorrhapha
Section: Schizophora
Superfamily: Diopsoidea
Family: Diopsidae
Billberg, 1820
Genera

Subfamily Centrioncinae

Subfamily Diopsinae

Synonyms
  • Centrioncidae [1]

Stalk-eyed flies are insects of the fly family Diopsidae. The family is distinguished from most other flies by most members of the family possessing "eyestalks": projections from the sides of the head with the eyes at the end. Some fly species from other families such as Drosophilidae, Platystomatidae, Richardiidae, and Tephritidae have similar heads, but the unique character of the Diopsidae is that their antennae are located on the stalk, rather than in the middle of the head as in all other flies. Stalked eyes are present in all members of the subfamily Diopsinae, but are absent in the Centrioncinae, which retain unstalked eyes similar to those of other flies. [2] The stalked eyes are usually sexually dimorphic, with eyestalks present but shorter in females. [3]

Contents

The stalk-eyed flies are up to a centimeter long, and they feed on both decaying plants and animals. Their unique morphology has inspired research into how the attribute may have arisen through forces of sexual selection and natural selection. Studies of the behavior of the Diopsidae have yielded important insights into the development of sexual ornamentation, the genetic factors that maintain such a morphological feature, sexual selection, and the handicap principle.

Distribution and habitat

More than 100 species in the Diopsidae are known, with the greatest diversity found in the Old World tropics. [4] They are distributed throughout the region, with the best-known species being from Southeast Asia and Southern Africa. Also, two species in North America have been described and a European species has recently been found in Hungary. [5]

Adult diopsids are typically found on low-lying vegetation in humid areas, often near streams and rivers, where they feed on fungi and bacteria, which they scavenge from decaying vegetation. The larvae are saprophagic or phytophagous, eating decaying and fresh plant matter. Diopsis macrophthalma Dalman, 1817, is a pest of rice and sorghum in tropical Africa.

The peculiar morphology of stalk-eyed flies makes it easy to identify their fossils (e.g. in amber); one fossil genus is Prosphyracephala, known from Eocene aged Baltic amber. [6] This genus has stalked eyes and is the earliest diverging member of the Diopsinae. [3]

Morphology

The Diopsidae are small to medium-sized flies, ranging from about 4.0 to about 12.0 mm in length. Their heads are subtriangular, with transverse eye stalks in all genera except the African genus Centrioncus and Teloglabrus . The head is usually sparsely haired, with vibrissae (whiskers) absent. [7]

The posterior portion of the fly's metathorax, or scutellum, 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. Adult males have lost tergites seven and eight, and the seventh sternite forms a complete ventral band. [7]

Stalk-eyed flies, as the name implies, typically possess eyestalks (in all but the two genera listed above). Their eyes are mounted on projections from the sides of the head, and the antennae are located on the eyestalks, unlike stalk-eyed flies from other families. Though both males and females of most species have eyestalks, they are much longer in males, a sexual dimorphism thought to be due to sexual selection. [8] A rather remarkable feature of stalk-eyed flies is their ability, 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. [9]

Taxonomy

True stalk-eyed flies are members of the family Diopsidae, first described by Fothergill [10] and named by Carl Linnaeus in 1775. [11] The family Diopsidae is contained within the order Diptera and suborder Cyclorrhapha, and features some 150 described species. [12]

The African genus Centrioncus (once placed in Sepsidae, but then moved to Diopsidae) was once recommended to be treated as a separate family, Centrioncidae, a sister group of the diopsids, [13] but since then this lineage has usually been treated as a subfamily. [14]

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, extensive binocular overlap occurs, with about 70% of the ommatidia of each eye having a binocular partner ommatidium in the opposite eye which views in the same direction. [15] [16] The binocular field is most extensive in the frontoventral quadrant, where it reaches over 135°, and is smallest in the dorsal region. 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 thread-like 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 mm, and reactions to model flies and reflections in a mirror also occur at about this distance. [15]

Mating

Male Teleopsis dalmanni Teleopsis dalmanni.jpg
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. [17] Male stalk-eyed flies with long eyestalks gain mating advantages both because of female choice and because they are better able to compete with rival males. [4] [18]

Sexual selection

Though the evolution of exaggerated male traits as a result of female mate choice was at one point controversial, the Diopsidae are now regarded as a classic example of animals that exhibit sexually selected traits. [8] [19] [20] 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. [21] [22] 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 natural selection against further trait elaboration balances sexual selection. [21]

Close-up of a male Teleopsis dalmanni Teleopsis dalmanni 2.jpg
Close-up of a male Teleopsis dalmanni

The extreme morphology exhibited by stalk-eyed flies (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-m stretch of stream bank to confirm this observation. [23]

Sexual selection experiments

Researchers 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. [24] Observations of 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 with the longest or shortest eye-span to body-length ratios were mated with 25 randomly chosen females. 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. [23]

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 finding supported the hypothesis that the change in female mate choice was genetically based and not learned. Thus, stalk-eyed flies have been able to evolve a sexual trait in males that corresponds directly to traits that affect mating choices made by females. [23]

Stalk-eyed fly (Diasemopsis) Stalk-eyed fly (Diasemopsis) (4561140578).jpg
Stalk-eyed fly ( Diasemopsis )

Handicap selection

However, the evolution of extreme morphology in male flies and the corresponding evolution of female preference for these characteristics as an effect of sexual selection is only half the picture. [25] Handicap models of sexual selection predict that male sexual ornaments have strong condition-dependent expression, and this allows females to evaluate male genetic quality. [26] [27] [28] [29] [30]

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. [25] Some male genotypes develop large eye spans under all conditions, whereas other genotypes progressively reduce eye spans as environmental conditions deteriorate. Several nonsexual 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, selected not only on the basis of attractiveness, but also because it demonstrates good genes in mates. [25]

Furthermore, some populations of stalk-eyed fly females carry a meiotic drive gene on their X chromosomes that causes female-biased sex ratios. [31] In these populations, males which carry a gene to suppress 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 sire more male offspring. [32] 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. [32]

Related Research Articles

<span class="mw-page-title-main">Sexual selection</span> Mode of natural selection involving the choosing of and competition for mates

Sexual selection is a mode of natural selection in which members of one biological sex choose mates of the other sex to mate with, and compete with members of the same sex for access to members of the opposite sex. These two forms of selection mean that some individuals have greater reproductive success than others within a population, for example because they are more attractive or prefer more attractive partners to produce offspring. Successful males benefit from frequent mating and monopolizing access to one or more fertile females. Females can maximise the return on the energy they invest in reproduction by selecting and mating with the best males.

<span class="mw-page-title-main">Lek mating</span> Type of animal mating behaviour

A lek is an aggregation of male animals gathered to engage in competitive displays and courtship rituals, known as lekking, to entice visiting females which are surveying prospective partners with which to mate. A lek can also indicate an available plot of space able to be utilized by displaying males to defend their own share of territory for the breeding season. A lekking species is characterised by male displays, strong female mate choice, and the conferring of indirect benefits to males and reduced costs to females. Although most prevalent among birds such as black grouse, lekking is also found in a wide range of vertebrates including some bony fish, amphibians, reptiles, and mammals, and arthropods including crustaceans and insects.

<span class="mw-page-title-main">Handicap principle</span> Hypothesis in evolutionary biology

The handicap principle is a hypothesis proposed by the Israeli biologist Amotz Zahavi to explain how evolution may lead to "honest" or reliable signalling between animals which have an obvious motivation to bluff or deceive each other.

<span class="mw-page-title-main">Fisherian runaway</span> Sexual selection mechanism

Fisherian runaway or runaway selection is a sexual selection mechanism proposed by the mathematical biologist Ronald Fisher in the early 20th century, to account for the evolution of ostentatious male ornamentation by persistent, directional female choice. An example is the colourful and elaborate peacock plumage compared to the relatively subdued peahen plumage; the costly ornaments, notably the bird's extremely long tail, appear to be incompatible with natural selection. Fisherian runaway can be postulated to include sexually dimorphic phenotypic traits such as behavior expressed by a particular sex.

<span class="mw-page-title-main">Reproductive success</span> Passing of genes on to the next generation in a way that they too can pass on those genes

Reproductive success is an individual's production of offspring per breeding event or lifetime. This is not limited by the number of offspring produced by one individual, but also the reproductive success of these offspring themselves.

<span class="mw-page-title-main">Platystomatidae</span> Family of flies

The Platystomatidae are a distinctive family of flies (Diptera) in the superfamily Tephritoidea.

<span class="mw-page-title-main">Mate choice</span> One of the primary mechanisms under which evolution can occur

Mate choice is one of the primary mechanisms under which evolution can occur. It is characterized by a "selective response by animals to particular stimuli" which can be observed as behavior. In other words, before an animal engages with a potential mate, they first evaluate various aspects of that mate which are indicative of quality—such as the resources or phenotypes they have—and evaluate whether or not those particular trait(s) are somehow beneficial to them. The evaluation will then incur a response of some sort.

<span class="mw-page-title-main">Sexy son hypothesis</span> Postulate in biology

The sexy son hypothesis in evolutionary biology and sexual selection, proposed by Patrick J. Weatherhead and Raleigh J. Robertson of Queen's University in Kingston, Ontario in 1979, states that a female's ideal mate choice among potential mates is one whose genes will produce males with the best chance of reproductive success. This implies that other benefits the father can offer the mother or offspring are less relevant than they may appear, including his capacity as a parental caregiver, territory and any nuptial gifts. Fisher's principle means that the sex ratio is always near 1:1 between males and females, yet what matters most are her "sexy sons'" future breeding successes, more likely if they have a promiscuous father, in creating large numbers of offspring carrying copies of her genes. This sexual selection hypothesis has been researched in species such as the European pied flycatcher.

<span class="mw-page-title-main">Lek paradox</span>

The lek paradox is the conundrum of how additive or beneficial genetic variation is maintained in lek mating species in the face of consistent sexual selection based on female preferences. While many studies have attempted to explain how the lek paradox fits into Darwinian theory, the paradox remains. Persistent female choice for particular male trait values should erode genetic diversity in male traits and thereby remove the benefits of choice, yet choice persists. This paradox can be somewhat alleviated by the occurrence of mutations introducing potential differences, as well as the possibility that traits of interest have more or less favorable recessive alleles.

<span class="mw-page-title-main">Courtship display</span> Communication to start a relationship with someone or to get sexual contact

A courtship display is a set of display behaviors in which an animal, usually a male, attempts to attract a mate; the mate exercises choice, so sexual selection acts on the display. These behaviors often include ritualized movement ("dances"), vocalizations, mechanical sound production, or displays of beauty, strength, or agonistic ability.

<span class="mw-page-title-main">Multiple sexual ornaments</span>

Many species have multiple sexual ornaments, whereby females select mating partners using several cues instead of only one cue. Whereas this phenomenon is self-evident and hence long recognized, adaptive explanations of why females use several instead of only one signal have been formulated relatively recently. Several hypotheses exist, but mutually exclusive tests are still lacking.

<span class="mw-page-title-main">Female sperm storage</span>

Female sperm storage is a biological process and often a type of sexual selection in which sperm cells transferred to a female during mating are temporarily retained within a specific part of the reproductive tract before the oocyte, or egg, is fertilized. This process takes place in some species of animals, but not in humans. The site of storage is variable among different animal taxa and ranges from structures that appear to function solely for sperm retention, such as insect spermatheca and bird sperm storage tubules, to more general regions of the reproductive tract enriched with receptors to which sperm associate before fertilization, such as the caudal portion of the cow oviduct containing sperm-associating annexins. Female sperm storage is an integral stage in the reproductive process for many animals with internal fertilization. It has several documented biological functions including:

A biological ornament is a characteristic of an animal that appears to serve a decorative function rather than a utilitarian function. Many are secondary sexual characteristics, and others appear on young birds during the period when they are dependent on being fed by their parents. Ornaments are used in displays to attract mates, which may lead to the evolutionary process known as sexual selection. An animal may shake, lengthen, or spread out its ornament in order to get the attention of the opposite sex, which will in turn choose the most attractive one with which to mate. Ornaments are most often observed in males, and choosing an extravagantly ornamented male benefits females as the genes that produce the ornament will be passed on to her offspring, increasing their own reproductive fitness. As Ronald Fisher noted, the male offspring will inherit the ornament while the female offspring will inherit the preference for said ornament, which can lead to a positive feedback loop known as a Fisherian runaway. These structures serve as cues to animal sexual behaviour, that is, they are sensory signals that affect mating responses. Therefore, ornamental traits are often selected by mate choice.

Phytalmia mouldsi is in the subfamily Phytalmiinae which includes all of the antlered fruit flies. They were discovered by M. S. Moulds in 1977 and are found only in an isolated rainforest of Australia. Antlered flies, collectively, are notable for their unique mating behavior and the unusual antler-like extensions on the heads of the males.

Interlocus sexual conflict is a type of sexual conflict that occurs through the interaction of a set of antagonistic alleles at two or more different loci, or the location of a gene on a chromosome, in males and females, resulting in the deviation of either or both sexes from the fitness optima for the traits. A co-evolutionary arms race is established between the sexes in which either sex evolves a set of antagonistic adaptations that is detrimental to the fitness of the other sex. The potential for reproductive success in one organism is strengthened while the fitness of the opposite sex is weakened. Interlocus sexual conflict can arise due to aspects of male–female interactions such as mating frequency, fertilization, relative parental effort, female remating behavior, and female reproductive rate.

<i>Sepsis cynipsea</i> Species of fly

Sepsis cynipsea is a European species of fly and member of the family Sepsidae. It is a coprophagous fly that feeds on dung. These flies are most commonly found around freshly laid cattle dung where they eat and reproduce. Due to human agricultural practices involving cows, these flies are now common in other areas of the world.

<i>Prochyliza xanthostoma</i> Species of fly

Prochyliza xanthostoma, the waltzing fly, is a species of carrion-feeding cheese skipper, insects in the family Piophilidae and the order Diptera. P. xanthostoma is a member of the genus Prochyliza, which contains eleven species. The adult flies are found through North America and are brown-bodied, with orange and black coloring. Mating occurs on animal carcasses and male perform mating rituals; females engage in ejaculate feeding. The waltzing fly is known for its exaggerated sexual dimorphism and has thus become a prominent model for sexual dimorphism and larval behavior. These organisms are known as cheese skippers because when startled, the larvae can leap several inches into the air. P. xanthostoma is an important model organism for sexual selection, larval behavior, and adult reproductive success and survivability.

Derocephalus angusticollis is a fly in the family Neriidae. They are typically found on the east coast of Australia near rotting vegetation. Aggregating on the rotting bark of trees such as Acacia longifolia and other trees in New South Wales and southern Queensland. D. angusticollis flies found in the wild have accelerated speeds of development and age of mortality when compared to those in captivity. Derocephalus One characteristic of the neriid fly is that it demonstrates sexual dimorphism. Males have a larger build as well as exaggerated physical characteristics such as wider heads and longer limbs. Certain phenotypic characteristics are dependent on the diet of the parents.

<i>Teleopsis dalmanni</i> Species of fly

Teleopsis dalmanni, synonym Cyrtodiopsis dalmanni, also known as the Malaysian stalk-eyed fly, is a species of fly in the family Diopsidae. T. dalmanni flies possess lateral elongations on their head capsules called eyestalks. These eyestalks play an important role in mate selection and as a result physical characteristic of the fly has been the subject of several studies on sexual selection, natural selection, and mating behavior.

<i>Richardia telescopica</i> Species of insect

Richardia telescopica is a species of flies from the genus Richardia. The species was originally described by Gerstaecker in 1860 and it occurs in Nicaragua, Costa Rica, and Panama.

References

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  32. 1 2 Zimmer, Carl (2008). "The Evolution of Extraordinary Eyes: The Cases of Flatfishes and Stalk-eyed Flies". Evolution: Education and Outreach. 1 (4): 487–492. doi: 10.1007/s12052-008-0089-9 .
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