''Scaptomyza flava'' is an herbivorous

leaf mining A leaf miner is any one of numerous species of insects in which the larval stage lives in, and eats, the leaf tissue of plants. The vast majority of leaf-mining insects are moths ( Lepidoptera), sawflies ( Symphyta, the mother clade of wasp ...

fly species in the family

Drosophilidae The Drosophilidae are a diverse, cosmopolitan family of flies, which includes species called fruit flies, although they are more accurately referred to as vinegar or pomace flies. Another distantly related family of flies, Tephritidae, are true f ...

. In Latin, '' flava'' means golden or yellow. The fly is amber to dark brown in color and approximately 2.5 mm in length. In Europe and New Zealand the

larva A larva (; plural larvae ) is a distinct juvenile form many animals undergo before metamorphosis into adults. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle. The ...

e are pests of plants in the order

Brassicales The Brassicales (or Cruciales) are an order (biology), order of flowering plants, belonging to the eurosids II group of dicotyledons under the APG II system. One character common to many members of the order is the production of glucosinolate (mu ...

, including arugula, brassicas, broccoli, Brussels sprouts, bok choy, cabbage, canola, cauliflower, horseradish, kale, kohlrabi, napa cabbage, nasturtium, radish, rapini, rutabaga, turnip,

wasabi Wasabi (Japanese: , , or , ; ''Eutrema japonicum'' or ''Wasabia japonica'') or Japanese horseradish is a plant of the family Brassicaceae, which also includes horseradish and mustard in other genera. The plant is native to Japan and the Russian ...

and watercress. In New Zealand, its range has expanded to include host species that are intercropped with salad brassicas, including

gypsophila ''Gypsophila'' () is a genus of flowering plants in the carnation family, Caryophyllaceae. They are native to Eurasia, Africa, Australia, and the Pacific Islands. More typically, ''S. flava'' is oligophagous within the Brassicales. ''Scaptomyza'' are unusual within the Drospophilidae because the group includes species that are truly herbivorous. Other herbivorous drosophilids include ''D. suzukii'', which attacks fruit very early during ripening (and so is a frugivore) and species within the genus ''

Lordiphosa ''Lordiphosa'' is a genus of fly in the family Drosophilidae. Species *''Lordiphosa acongruens, L. acongruens'' (Zhang & Liang, 1992) *''Lordiphosa acuminata, L. acuminata'' (James Edward Collin, Collin, 1952) *''Lordiphosa alticola, L. alticola ...

'', from Africa and Asia, which also include leaf miners. Most drosophilids feed on microbes associated with decaying vegetation and sap fluxes.

Distribution

''Scaptomyza flava'' is

Holarctic The Holarctic realm is a biogeographic realm that comprises the majority of habitats found throughout the continents in the Northern Hemisphere. It corresponds to the floristic Boreal Kingdom. It includes both the Nearctic zoogeographical region ...

in distribution, commonly found across

Europe Europe is a large peninsula conventionally considered a continent in its own right because of its great physical size and the weight of its history and traditions. Europe is also considered a Continent#Subcontinents, subcontinent of Eurasia ...

Asia Asia (, ) is one of the world's most notable geographical regions, which is either considered a continent in its own right or a subcontinent of Eurasia, which shares the continental landmass of Afro-Eurasia with Africa. Asia covers an area ...

and

North America North America is a continent in the Northern Hemisphere and almost entirely within the Western Hemisphere. It is bordered to the north by the Arctic Ocean, to the east by the Atlantic Ocean, to the southeast by South America and the Car ...

and only recently has been discovered in

New Zealand New Zealand ( mi, Aotearoa ) is an island country in the southwestern Pacific Ocean. It consists of two main landmasses—the North Island () and the South Island ()—and over 700 smaller islands. It is the sixth-largest island count ...

, where it was first mistaken as a leaf mining agromyzid. The genus '' Scaptomyza'' contains species found on all continents except

Antarctica Antarctica () is Earth's southernmost and least-populated continent. Situated almost entirely south of the Antarctic Circle and surrounded by the Southern Ocean, it contains the geographic South Pole. Antarctica is the fifth-largest contine ...

Phylogeny

''Scaptomyza flava'' belongs to the order

Diptera Flies are insects of the order Diptera, the name being derived from the Greek δι- ''di-'' "two", and πτερόν ''pteron'' "wing". Insects of this order use only a single pair of wings to fly, the hindwings having evolved into advanced ...

, the family

, and the genus '' Scaptomyza'' along with around 272 other species. '' Scaptomyza'' is a

monophyletic In cladistics for a group of organisms, monophyly is the condition of being a clade—that is, a group of taxa composed only of a common ancestor (or more precisely an ancestral population) and all of its lineal descendants. Monophyletic gro ...

genus nested within the

paraphyletic In taxonomy (general), taxonomy, a group is paraphyletic if it consists of the group's most recent common ancestor, last common ancestor and most of its descendants, excluding a few Monophyly, monophyletic subgroups. The group is said to be pa ...

Drosophila ''Drosophila'' () is a genus of flies, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or (less frequently) pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species ...

'' lineage that includes ''D. mojavensis'', ''D. virliis'' and ''D. grimshawi''. The genus ''Scaptomyza'' is sister to or paraphyletic with respect to the Hawaiian ''Drosophila'' radiation. ''Scaptomyza flava'' is a member of the subgenus ''Scaptomyza'', which is the only subgenus in the ''Scaptomyza'' known to include obligate leaf mining species. However, ''S. flavella,'' in the subgenus ''Bunostoma'', is a facultative leaf miner of New Zealand sea celery, but adult females oviposit in decaying leaves and so living leaves are attacked by larvae that move in from decaying leaves. ''Scaptomyza flava'' was originally described as ''Drosophila flava'' in 1823, but later was redescribed as ''Scaptomyza flava'' when the genus ''Scaptomyza'' was erected (based on morphological differences with other ''Drosophila'', including longer wings relative to the length of the body). The species has also previously been referred to as ''S. apicalis'' and ''S. flaveola''. The most closely related living relative of ''S. flava'' is ''S. montana'', which forms a clade sister to ''S. nigrita''. More distantly related to the mustard-feeding ''Scaptomyza'' is ''S. graminum'', which feeds on Caryophyllaceae.

Life history

Life cycle

In captivity, the duration of the ''Scaptomyza flava'' life cycle is approximately three weeks, with an average egg to adult growth period of around 20.52 days. The length of the life cycle is over two times as long as yeast-feeding ''Drosophila'' like ''D. melanogaster'', a difference likely due to the fact that leaves are less nutritious and mount a potent chemical defense response against the eggs and leaf mining larvae. Like other adult females in the subgenus ''Scaptomyza,'' have highly sclerotized (hardened and darkened) ovipositors valves that are studded with 20-30 tooth-like sensilla. The dentate ovipositors are used both as a trophic organ and an egg-laying organ. To make a hole, the females crawl to the lower side of the leaf and using the blunt end of the ovipositor, move the two valves from side to side, carving a hole (also called a stipple) in the leaf, usually leaving the upper epidermis intact. Once retracting the ovipositor from the wound, they turn counter-clockwise and extend the proboscis to drink the juice that seeps into the wound. Adult females often have green abdomens as a result. Eggs are laid in feeding punctures introduced to the host plant by the female. Larvae hatch somewhere around 48 hours after the female deposits the eggs in the puncture. Once hatched, the larvae feed on the mesophylll tissue within the leaves and make a serpentine mine as they make their way toward the petiole and create a blotch mine as they mature (completing two more molts was a larvae) or move to a new leaf. Most individuals remain in the same plant through multiple stages of development. The larvae then either remain in the leaves or pupariate in the soil. Scaptomyza flava female

Mating

''Scaptomyza flava'' participate in

anisogamous Different forms of anisogamy: A) anisogamy of motile cells, B) egg_cell.html"_;"title="oogamy_(egg_cell">oogamy_(egg_cell_and_sperm_cell),_C)_anisogamy_of_non-motile_cells_(egg_cell_and_spermatia)..html" ;"title="egg_cell_and_sperm_cell.html" ;" ...

mating, like most animals. When males are exposed to females in a laboratory setting, they take two to three minutes to begin mating rituals. Generally, a male approaches a female and in a display of

courtship Courtship is the period wherein some couples get to know each other prior to a possible marriage. Courtship traditionally may begin after a betrothal and may conclude with the celebration of marriage. A courtship may be an informal and private m ...

flaps his wings and touches her body with his front legs. Females then become stationary as the male mounts her, and

copulation Sexual intercourse (or coitus or copulation) is a sexual activity typically involving the insertion and thrusting of the penis into the vagina for sexual pleasure or reproduction.Sexual intercourse most commonly means penile–vaginal penetrat ...

ensues. Uninterrupted copulation typically lasts around twenty minutes. After mating, the males vibrate their wings and leave the female behind, showing no further interest. Mating displays differed in frequency between mated and virgin males. Mated males are significantly more likely to practice courtship behavior and successfully mate than virgin flies. This suggests that male ''S. flava'' are capable of learning from previous mating experience. This behavior has also been reported in the distantly-related ''D. melanogaster''. In the lab, 90% of flies will mate once or twice, with a much smaller percentage mating three or more times. The mating patterns of ''S. flava'' are linked to their

circadian rhythm A circadian rhythm (), or circadian cycle, is a natural, internal process that regulates the sleep–wake cycle and repeats roughly every 24 hours. It can refer to any process that originates within an organism (i.e., Endogeny (biology), endogeno ...

Oviposition and fertility

''Scaptomyza flava'' begin

oviposition The ovipositor is a tube-like organ used by some animals, especially insects, for the laying of eggs. In insects, an ovipositor consists of a maximum of three pairs of appendages. The details and morphology of the ovipositor vary, but typical ...

approximately 2.7 days after emergence, with peak oviposition happening somewhere between five and ten days post-emergence. Over a lifetime, the average female produced approximately 130 eggs, of which approximately 71 were fertilized. Both oviposition and

fertility Fertility is the capability to produce offspring through reproduction following the onset of sexual maturity. The fertility rate is the average number of children born by a female during her lifetime and is quantified demographically. Fertili ...

peak within the first five to ten days post-emergence, with approximately 50% of the viable eggs are laid within the first 14 days from when the female began ovipositing.

Food sources

Diet

''Scaptomyza flava'' larvae are herbivorous endoparasites because they live in, consume and complete their entire immature development in the leaves of living plants. The adult females, like those of Agromyzidae, are also herbivores because they create feeding punctures with their ovipositors and feed on the leaf exudates that seep into the wounds.

Larvae

''Scaptomyza flava'' larvae are dependent on living plants as a food source, as opposed to other herbivorous insects that can digest decaying plant matter. ''Scaptomyza flava'' larvae live in and feed on plants in the Brassicales. Most other drosophilids feed on a mixture of yeast, bacteria and decaying plant tissue and can be reared on media containing yeast, but ''S. flava'' does not complete development on these or any other media tested. The trophic level of ''S. flava'' is more similar to a fluid-feeding aphid based on highly depleted nitrogen profiles. One benefit of this behavior is protection from

pathogen In biology, a pathogen ( el, πάθος, "suffering", "passion" and , "producer of") in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a germ ...

s, but this comes at the price of increased susceptibility to parasitoid attack. On the other hand, the plant also mounts a massive increase in defensive chemical concentrations after perceiving attack by ''S. flava'' though the plant's asmonate pathway. Downstream of the jasmonate pathway are genes involved in the biosynthesis of

glucosinolate Glucosinolates are natural components of many pungent plants such as mustard, cabbage, and horseradish. The pungency of those plants is due to mustard oils produced from glucosinolates when the plant material is chewed, cut, or otherwise damaged. T ...

s, which are upregulated after attack. Some glucosinolates (aliphatic) break down into stable mustard oils (

isothiocyanate In organic chemistry, isothiocyanate is the functional group , formed by substituting the oxygen in the isocyanate group with a sulfur. Many natural isothiocyanates from plants are produced by enzymatic conversion of metabolites called glucosinol ...

s), which persist in the environment (and are found in wasabi), but they are highly electrophilic, toxic molecules that rapidly bind to DNA and cysteine and lysine residues in cells. Both ''S. flava'' and ''D. melanogaster'' use the mercapturic acid pathway, like humans, to detoxify mustard oils. However, the glutathione ''S''-transferase enzymes in the ''Scaptomyza'' species that feed on Brassicales are more efficient than any known from any animal at detoxifying mustard oils. Stellwaag 00143a01

Adult

Adult females also feed on the same plants as the larvae. Instead of eating the plants from the inside out, however, they feed on the plant secretions induced by the punctures they make with their

ovipositor The ovipositor is a tube-like organ used by some animals, especially insects, for the laying of eggs. In insects, an ovipositor consists of a maximum of three pairs of appendages. The details and morphology of the ovipositor vary, but typical ...

Evolution of herbivory

Herbivory A herbivore is an animal anatomically and physiologically adapted to eating plant material, for example foliage or marine algae, for the main component of its diet. As a result of their plant diet, herbivorous animals typically have mouthpart ...

is not unique to the genus ''Scaptomyza'': one third of the living insect orders include herbivorous species and one-half of all living insect species are herbivorous. Thus, herbivory is the most successful life history from an evolutionary perspective. In the Diptera, herbivory has evolved at least 25 times independently. Specifically, herbivory in ''Scaptomyza'' is expected to have evolved between six and sixteen million years ago, with the most recent estimates placing this evolutionary event at approximately 13.5 million years ago. Most species of ''Scaptomyza'' are not herbivorous and over half of all living species (but no known leaf-miners) are native to Hawaii where they have diverse life histories, from spider egg sac parasitoids to leaf breeding (feeding on microbes and even perhaps dead arthropods trapped on sticky surfaces). Molecular phylogenetic analyses suggest herbivory evolved only once in the genus ''Scaptomyza''. Other species in the family Drosophilidae have a strong affinity for detecting the odors of

yeast Yeasts are eukaryotic, single-celled microorganisms classified as members of the fungus kingdom. The first yeast originated hundreds of millions of years ago, and at least 1,500 species are currently recognized. They are estimated to constitut ...

, a trait that ''S. flava'' has lost evolutionarily because its lineage has lost three genes encoding odorant receptors (ORs) that are known in ''D. melanogaster'' to be tuned to alilphatic esters produced by yeast. When the genes encoding these ORs are knocked out in ''D. melanogaster'' the flies may not orient properly toward these volatiles. The loss of ability to sense yeast is associated with evolutionary events leading to the evolution of herbivory. Adult female ''S. flava'' are attracted to volatile mustard oils, like most specialists of Brassicales plants, which have co-opted these toxic chemicals as indicators of their host plants. ORs encoded by recently duplicated ''Or67b'' genes that evolved rapidly in the ''S. flava'' lineage were found to be tuned to volatile mustard oils, which are emitted by wounded Brassicales plants. A similar phenomenon occurred independently in the diamondback moth ''Plutella xylostella''. When one of these ORs, ''Or67b,'' is expressed in two different olfactory circuits in ''D. melanogaster'', flies are attracted to mustard oils, which is not typical for ''D. melanogaster''. This suggests that ''S. flava Or67b,'' when artificially expressed in a distant relative that feeds on yeast in rotting fruit, can result in a attraction behavior to mustard oils, possibly explaining how specialization on toxic plants can occur through simple genetic changes. Methyl salicylate, a derivative of the ubiquitous plant hormone salicylic acid, is also known to attract ''S. flava'' flies at traps in New Zealand. ''S. flava'' is not captured at traps baited with bananas and yeast. Most drosophilids, especially those associated with rotting fruit, encounter ethanol and have evolved mechanisms for tolerating and even using it to combat parasitoids. Although drosophilds vector yeast and may be mutualists, the plants attacked by ''Scaptomyza'' are harmed by these flies. As a result they mount a rapid chemical defense to render the food and habitat an inhospitable environment after wounding is detected. When the jasmonate or glucosinolate pathways are knocked out in host plants, ''S. flava'' larvae perform better, suggesting that these pathways are involved in a level of resistance to the flies. Conversely, when plants are pre-treated with jasmonate, larvae perform worse.

Bypassing glucosinolates

The species ''S. flava'' and ''S. nigrita'' have evolved the ability to partially metabolize the hydrolysis products of glucosinolates, which include the isothiocyanates, and are toxic chemicals synthesized by mustard plants and relatives as a defense mechanism. Other species in the family Drosophilidae are largely unable to overcome these toxins. Glucosinolates play a role in regulating stress-related genes in ''S. flava,'' which is different from the specialized systems that other herbivores have developed to bypass the toxic effect of the chemical.

Mutualism

''Scaptomyza flava'' adult females and larvae

inoculate Inoculation is the act of implanting a pathogen or other microorganism. It may refer to methods of artificially inducing immunity against various infectious diseases, or it may be used to describe the spreading of disease, as in "self-inoculati ...

their host plants with bacteria to aid in the feeding process. Specifically, ''S. flava'' may introduce ''

Pseudomonas syringae ''Pseudomonas syringae'' is a rod-shaped, Gram-negative bacterium with polar flagella. As a plant pathogen, it can infect a wide range of species, and exists as over 50 different pathovars, all of which are available to researchers from internat ...

'' to the host plant, which interferes with the anti-herbivore defenses of the host plant. Both adult females and larvae are capable of acting as bacterial vectors. ''Scaptomyza flava'' larvae not only prefer to eat plants infected with ''P. syringae'', but have actually been shown to develop faster when feeding on infected plants. The relative ''S. nigrita'' has a complex association with phyllosphere bacteria, that likely includes antagonisms, mutualisms, and commensalisms between the leaf miner and microbes.

Horizontal gene transfer

Genes encoding bacterial or phage-derived toxins have been identified in the genome sequence of ''S. flava''. These genes were previously found to be associated with APSE phage toxin cargo genes that confer resistance to parasitoid wasp attack when the phage genes are found in endosymbiotic bacteria that infect aphids.

Interactions with humans

''Scaptomyza flava'' feed on various agricultural staples, often damaging the plants in which they live. While heavy infestations on various food crops can reduce yields, specific measures are not usually taken to contain the fly.

As a model organism

''Scaptomyza flava'' is being developed as a model to study the interactions between plants and herbivorous arthropods. Because it is relatively closely related to the "fruit fly" ''Drosophila melanogaster'', the evolution of genes in its genome are more readily characterized. Specific genetic changes that have evolved and are involved in the adaptation to feeding on living plants can be more easily identified as a result. The fly attacks ''Arabidopsis thaliana'' in nature and because this host plant is the premier plant model organism, the genes important in mediating the interaction with ''S. flava'', particularly those involved in resistance, can be studied readily.

References

External links

Images representing ''Scaptomyza flava''
at

BOLD In typography, emphasis is the strengthening of words in a text with a font in a different style from the rest of the text, to highlight them. It is the equivalent of prosody stress in speech. Methods and use The most common methods in W ...

{{Taxonbar, from=Q13851757 Drosophilidae Insects described in 1823 Muscomorph flies of Europe Taxa named by Carl Fredrik Fallén