Caenocholax fenyesi

Caenocholax fenyesi is a species of twisted-winged parasitic insects in the order Strepsiptera and family Myrmecolacidae.[1] It has a sporadic distribution throughout North America, Central America, and South America.[2] Chaenochlax brasiliensis (Oliveira and Kogan 1959) is the only other named species in the genus.[1]

Caenocholax fenyesi
Scientific classification
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Strepsiptera
Family: Myrmecolacidae
Genus: Caenocholax
Species:
C. fenyesi
Binomial name
Caenocholax fenyesi
Pierce, 1909

C. fenyesi displays heterotrophic heteronomy, where males and females occupy different hosts.[3][2] Females are endoparasites throughout their lifecycle and parasitize members of Orthoptera, while larval stage males are endoparasites of Solenopsis invicta, the red imported fire ant, and are free-living as adults.[3][1] Males in Arizona, Mexico, Central America, and parts of South America have performed a host switch and parasitize native fire ants closely related to S. invicta.[1] They are highly virulent in their adult hosts, but not in their larval hosts due to a slower growth rate in larval stages.[4]

Taxonomy

Subspecies are cryptic and are morphologically similar, but genetically different.[5] These three subspecies belong to the species Caenocholax fenyesi:[5]

Phylogeny and Genetic Structure

Phylogenetic relationships are inferred based on the morphology of adults and specific host associations.[1] Cryptic diversity and genetic divergence over large distances have been observed, causing an effect of genetic bottlenecking.[4][3] This makes the extinction of C. fenyesi highly probable, but new populations may become established when mated larvae successfully disperse larvae across long distances.[3]

Distribution

C. fenyesi is distributed throughout the southern United States, Central America, and South America.[2] Overall distribution in the United States includes Florida, New Orleans, southern and central Louisiana, Mississippi, Georgia, Arizona, Alabama, and Texas.[2] In the Neotropics, they are found in Cordoba, Mexico; Tabasco, Mexico; Peten, Guatemala; Metagalpa, Nicaragua; Costa Rica; Panama; Ecuador; Chile; Missiones, Argentina; Andros Island, Bahamas; and Cuba.[2] Individuals live in small numbers in close proximity due to the adult male's short lifespan.[3]

Habitat

Because males and females parasitize different insects, their respective habitats depend on host preferences and the intersection of the habitat and range of their different hosts.[3][2] Males, along with their ant hosts, are less common in grassland habitats.[2] There is not enough time for males to develop, establish, and occupy their own unique habitat.[2]

Local dispersal allows C. fenyesi to persist in a small area.[3] However, dispersal of larvae is extremely restricted because reproducing females must depend on a new orthopteran host for the larvae.[3] Males depend on a new ant host, which are difficult to find because ants usually stay close to their nest[3]. Poorly developed flight and short lifespans also constrain dispersal by males.[3] Overall, dispersal of male first instar larvae is extremely limited because adult and nymph stages of the ant host live within the same habitat.[5]

Reproduction and Development

Sexual selection in C. fenyesi occurs via sensory exploitation.[6] Females are not choosy about mates, but males are choosy and will show no interest in copulation or mating if a female is currently carrying embryos at an advanced stage of development.[6] If the male is unsuccessful at stimulating the female during courtship, she will reject him.[6] The head is the only part on the female's body that the male has contact with during insemination.[6]

Generalized Lifecycle

Females do not have a pupal instar stage.[4] Oocytes float freely in her haemolymph and she may produce up to 750,000 embryos.[4] Fertilization occurs by means of haemocoelic insemination and reproduction occurs by means of haemocoelous viviparity.[4] Motile first instar larvae are released through the brood canal opening in the female's cephalothorax.[3] When males find their ant host, the first instar larvae go through hypermetamorphosis, bore through the cuticle, and moult into the second instar larvae.[5][1]

Males moult several times and develop according to the following stages:[4]

  1. Prepupa: Prefrontal nervous system develops and complex eyes and wings develop further.
  2. Pupa: Wings and genitalia grow to full size.
  3. Subimago: Wings remain in their sheath.
  4. Imago: Cuticles from the prepupal, pupal, and subimaginal stages are shed; wings are fully inflated and flight muscles are developed; sperm matures.

Males emerge from the host when they reach adulthood and immediately begin to fly and search for a female to mate with.[5] Their adult lifespan is usually a few hours, but may be up to a few days.[2]

Copulation

Females send out sex hormones to attract a male[6]. The male strikes the female's cephalothorax with his tarsi during courtship to stimulate her[6]. Copulation may occur for up to a minute and multiple times before the male begins searching for another female to mate with[6].

Parasitism

Each host is occupied by one individual.[1] The first instar larvae of males must reach an ant colony to parasitize larvae and pupae, which is accomplished by travelling with a foraging ant.[1] This gives them a host with a long enough lifespan for development.[1] As koinobionts, the host of C. fenyesi continues to develop after parasitization.[7] The host's life is lengthened to allow males to mature and females to release the first instar larvae when the next generation of the host's larvae are produced.[5] The original host was assumed to be the black fire ant (Solenopsis richteri) in MesoAmerica, which switched to the red imported fire ant in the southern United States.[8]

Anatomy

Males and females of C. fenyesi are sexually dimorphic.[1] There are four larval stages, but only three have been described.[4][1] Larval stages are named secondary and tertiary stages based on morphological characteristics, but are not necessarily sequential stages.[1] Endoparasitic larval stages experience apolysis, but no ecdysis.[1] First instar larvae are free-living, while secondary and tertiary larvae are endoparasitic in both males and females.[1] The sex of individuals can be determined by the time they reach the second instar stage.[4] By the third instar stage, males have three pairs of prolegs and a bulbous head; while females have a rounded "head" region and tapering abdomen.[4] The first four abdominal segments have sensory bristles in all larval stages.[1]

First Instar Larvae

The function of the first instar is to find a suitable host.[4] Physical environmental conditions affect the lifespan at this stage, so it is short-lived.[5] At this stage, individuals have a scleratized cuticle and are brown and 70-80 um long, not including the caudal filaments.[4][1] Ventral regions of the head, thorax, and abdomen are serrated, and dorsal and lateral surfaces are mainly smooth.[4][1] Legs are slender and spined, and tarsi have single joints, no claws, and ventral modifications to resemble adhesive pads.[4][1]

There are three pairs of pits on the dorsal surface of the head.[1] There are three ocelli 3-4 um in diameter; one located ventrally and two dorsally/ventrally.[1] There is a distinct invagination on the median anterior margin.[1] Antennae are positioned lateral to the mouth and appear filliform but have also been described as having three segments with a long arista on the second segment.[1]

Each segment of the thorax has spiny sternal sclerites, a pair of dorsal pits, and a ventral-lateral pair of pits.[1] Some spines and serrations extend from the edge of the segment on the ventral side[1]. Tarsi on the legs of the prothorax and mesothorax have pads.[1] The metathorax has three finger-like projections anteriorly to each coxa.[1]

The abdomen has 10 segments with short, spiky projections on the lateral surface and serrations, spines, and two pairs of setal bristles on the ventral surface.[1] Segments 1-4 have a pair of ventral-lateral setaceous spines that are 4.5 um long[1]. Segments 4-7 each have a pair of 0.5-1.5 um-long spines on the ventral posterier edge.[1] Segments 7-10 have small, broad serrations on the posterior sternum ventrally.[1] There are two pairs of bristly lateral/dorsal setae 11 um long on segment 9 and one pair of 40. um-long caudal filaments on segment 10, which are used for jumping.[1]

Secondary Larvae

Individuals at this stage are 200-350 um in size and light brown, with a rounded head and membraneous cuticle.[1] There are 13 differentiated segments, but the last two segments are narrower than the others.[1]

Tertiary Larvae

This stage is similar to the secondary larva, but individuals are much larger at 600-700 um in size, and the head is less rounded and cap-like with a broadly pointed anterior end.[1]

Adult Female Anatomy

Females are wingless, eyeless, and possess no antennae, mouthparts, legs, or external genitalia.[7][6] They are relatively large in size at 1.5-3.9 mm.[9][7] Female first instar larvae are 0.89 mm long.[9] The female's head is vestigial and is fused to the reduced, indistinct segments of the thorax.[6] The mandibles have several spines on the inner surface.[9] The cephalothorax is 0.55 mm long and 0.43 mm wide, light brown, and lies flat on the host's abdomen and extrudes through the host's abdominal pleurites.[9] The brood canal opening is 0.18 mm long and 0.33 mm wide.[9] The second and third abdominal segments have a genital aperture.[9]

Adult Male Anatomy

Males range in size from 1.5 to 6 mm.[7] They have short forewings and large, fan-like hindwings with reduced venation.[4][3] Eyes have 15-150 individual ommatidia separated by bridges covered with microtrichia.[10][4] Mouthparts are blade-like mandibles and maxillae.[4] Males have an inconspicuous prothorax.[4] Fore and midlegs have no trochanters and tarsi have 2-5 segments.[4] There are spines on the tarsi, tibia, and femora on all pairs of legs and the tibia and femora are larger on the third pair of legs.[1] The aedeagus is located on the ninth abdominal segment and is overhung by the tenth segment.[4]

Biological Control in Red Imported Fire Ants (S. invicta)

C. fenyesi has been suggested as a potential agent for the biological control of the red imported fire ant, S. invicta in the United States and Australia[9]. When parasitized by C. fenyesi, red imported fire ants climb to a high perch and assume a gaster flagging posture and remain in this position until C. fenyesi emerges.[2]

S. invicta was introduced into the United States from South America in the early 1900s and have since expanded their range to cover more than 129.5 million hectares.[11] Chemical insecticides are commonly used for controlling their populations but because S. invicta has no natural enemies in North America, this is only a temporary solution and many biological control agents have been suggested.[11] However, this parasite of fire ants has a low rate of parasitization and currently more research is required to determine if C. fenyesi can be used as a reliable biocontrol of S. invicta.[11]

References
  1. Cook, J. L., Vinson, S. B., Gold, R. E. (1998). "Developmental stages of Caenocholax fenyesi Pierce (Strepsiptera : Myrmecolacidae) : Descriptions and significations to the higher taxonomy of Strepsiptera". International Journal of Insect Morphology and Embryology. 27: 21–26. doi:10.1016/S0020-7322(97)00030-5.CS1 maint: multiple names: authors list (link)
  2. Cook, J. L., Johnston, J. S., Gold, R. E., Vinson, S. B. (1997). "Distribution of Caenocholax fenyesi (Strepsiptera : Myrmecolacidae) and the Habitats Most Likely to Contain Its Stylopized Host, Solenopsis invicta (Hymenoptera: Formicidae)". Environmental Entomology. 26 (6): 1258–1262. doi:10.1093/ee/26.6.1258.CS1 maint: multiple names: authors list (link)
  3. Hayward, A., Mcmahon, D. P., Kathirithamby, J. (2011). "Cryptic diversity and female host specificity in a parasitoid where the sexes utilize hosts from separate orders". Molecular Ecology. 20 (7): 1508–1528. doi:10.1111/j.1365-294X.2011.05010.x. PMID 21382110. S2CID 25161682.CS1 maint: multiple names: authors list (link)
  4. Kathirithamby, J. (2005). "Strepsiptera (Insecta) of Mexico - A Review". Monograph. 12: 103–118.
  5. Kathirithamby, J. (2009). "Host-parasitoid Associations in Strepsiptera". Annual Review of Entomology. 54: 227–249. doi:10.1146/annurev.ento.54.110807.090525. PMID 18817508.
  6. Kathirithamby, J., Hrabar, M., Delgado, J. A., Collantes, F. (2015). "We do not select, nor are we choosy: Reproductive biology of Strepsiptera (Insecta)". Biological Journal of the Linnean Society. 116: 221–238. doi:10.1111/bij.12585.CS1 maint: multiple names: authors list (link)
  7. Johnston, J. S., Ross, L. D., Beani, L., Hughes, D. P., Kathirithamby, J. (2004). "Tiny genomes and endoreduplication in Strepsiptera". Insect Molecular Biology. 13 (6): 581–585. doi:10.1111/j.0962-1075.2004.00514.x. PMID 15606806. S2CID 30816756.CS1 maint: multiple names: authors list (link)
  8. Kathirithamby, J., Hughes, D. P. (2002). "Caenocholax fenyesi (Strepsiptera: Myrmecolacidae) Parasitic in Camponotus planatus (Hymenoptera: Formicidae) in Mexico: Is This the Original Host?". Annals of the Entomological Society of America. 95 (5): 558–563. doi:10.1603/0013-8746(2002)095[0558:CFSMPI]2.0.CO;2.CS1 maint: multiple names: authors list (link)
  9. Kathirithamby, J., Johnston, J. S. (2004). "The Discovery after 94 Years of the Elusive Female of a Myrmecolacid (Strepsiptera), and the Cryptic Species of Caenocholax fenyesi Pierce Sensu Lato". Proceedings: Biological Sciences. 271: S5–S8. doi:10.1098/rsbl.2003.0078. PMC 1809985. PMID 15101403.CS1 maint: multiple names: authors list (link)
  10. Pohl, H., Beutel, R. G. (2005). "The phylogeny of Strepsiptera (Hexapoda)". Cladistics. 21 (4): 328–274. doi:10.1111/j.1096-0031.2005.00074.x. S2CID 85267294.CS1 maint: multiple names: authors list (link)
  11. Williams, D. F., Porter, S., Pereira, R. M. (2003). "Biological Control of Imported Fire Ants (Hymenoptera: Formicidae)". American Entomologist. 49 (3): 150–163. doi:10.1093/ae/49.3.150.CS1 maint: multiple names: authors list (link)

Further reading
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