Thursday, May 31, 2018

Antiplacentas and Incestuous Teratomata: Reproductive Weirdness among the Coccoids

Picture of a virtual bilateral gynandromorph of the eastern tiger swallowtail Papilio glaucus
Gynandromorph of Papilio glaucus (M=L/F=R), photographed by James Adams
A valid dictum of biology could be that for nearly every law, as per a field like physics or mathematics, there will be at least one exception. One of these dicta is that the Insecta are strictly dioecious: that is, male and female gametes are never produced by the same individual. Teratogenic exceptions are of course sometimes documented (of which bilateral gynandromorphs are the most visually notable), but the sheer rarity of hermaphroditic hexapods is striking, particularly when one considers that the frequency of this phenomenon throughout the rest of the Pancrustacea* (Juchault, 1999; Normark, 2002) and Metazoa as a whole.

tiny insects? on scales - Icerya purchasi
Cluster of Icerya purchasi photographed by Colette Micallef (host plant unspecified)
Indeed, the only known hermaphroditic insects are three species in the economically significant coccoid genus Icerya (Hemiptera: Sternorrhyncha: Coccoidea: Monophlebidae), including I. purchasi, the cottony cushion scale of agricultural infamy (Royer, 1975). Phylogenetic inferences imply that these lineages each independently developed hermaphroditism (Unruh & Gullan, 2008). However, the often-cited factoid of hermaphroditic monophlebids does not hold up to developmental scrutiny: the reality of reproduction in these Icerya spp. is far more peculiar.

You thought that the life cycle of Micromalthus debilis was complicated? Get a load of this
Unprepossessing but speciose, the Coccoidea as a whole are remarkable for a trend towards paedomorphy and immobility among females, with males correspondingly becoming minute and non-feeding. They are even more remarkable in that this one clade encapsulates the entire diversity of sexual systems known in the Insecta (Ross et al., 2012), with the supposed ancestral condition of sex determination being XX-XO (see flowchart of transitions between these character states at left from Ross et al., 2010), but in several lineages of Icerya, sex determination is haplodiploid: males develop from unfertilized (haploid) eggs, whereas females are diploid (Ross et al., 2010). This fact is integral to comprehending the reproductive realities of these putative hermaphrodites. 

In I. purchasi, males are rare but not unknown; the bulk of the population (>90%) consists of self-fertilizing "hermaphrodites" in functional terms, but females in fact (Hughes-Schrader, 1925), with spermatozoa produced by haploid tissue (Royer, 1975). In the case of I. purchasi, at least, this haploid tissue is established from excess parental sperm, which, rather than fertilize oocytes, establish themselves transovarially in female oocysts and proliferate within diploid female tissues. As Normark (2003) put it, "hermaphroditism may be an inadequate term with which to describe this situation." Rather, female cottony cushion scales are infected with a vertically-transmitted clonal lineage of males reduced to a germ line. I. purchasi females breed with this "permanent cancer of the[ir] germ line" (Normark, 2003), which due to the lack of recombination inherent in haploid males' conception is (in genetic terms) their own father incarnate as a teratoma.

Schematic of reproductive possibilities in hermaphroditic Icerya spp. (Gardner & Ross, 2011)
While bizarre, this arrangement need not require a listen to the original soundtrack to "Annihilation" (2018) and a hallucinogenic drug of one's choice to make adaptive sense. (Although both actions are appropriate responses.) From an inclusive-fitness perspective, the male germlines of Icerya maximize their fitness by cloning themselves and obligately inbreeding with their female descendants (Gardner & Ross, 2011), with scope for both competition and collaboration between females and infectious male tissues.

Icerya does not contain the only examples of dizygotic (Gavrilov & Kuznetsova, 2007) tissue in coccoids, although the other two examples have an entirely separate adaptive justification: namely, to vertically transmit bacteriomes, a descriptive term referring to specialized tissues (consisting of bacteriocytes) that withhold endosymbionts. In Sternorrhyncha, it is generally assumed that these bacteria provide essential amino acids absent from a diet (plant sap) that consists almost exclusively of polysaccharides (Thao et al., 2002). In the monobasic (Hodgson and Hardy, 2013) Putoidae, which unlike Icerya are diplodiploid (Hughes-Schrader, 1944), maternal bacteriocytes invade the nascent embryo and propagate therein, bacteria and all (Buchner, 1965), thus giving rise to a bacteriome of maternal tissue. Cytogenesis that has dizygotic products is termed Schrader fusion (Gavrilov & Kuznetsova, 2007).

β-(blue) and γ-(red) proteobacteria, both without (L) and within (R) Planococcus citri oocyte
Conversely to the Putoidae, the Diaspididae (Gavrilov & Kuznetsova, 2007) and at least some true mealybugs (Pseudococcidae) engage in Schrader fusion involving the oocyte's polar bodies (which degenerate in the remainder of the Metazoa), again as a means of creating bacteriomes (Normark, 2003). Typical mealybugs host β-proteobacterial endosymbionts (Candidatus Tremblaya princeps in Pseudococcinae, Candidatus T. phenacola in Phenacoccinae; López-Madrigal et al., 2015) (contrasting with the γ-proteobacteria that generally act in this digestive context throughout the Insecta; Moran & Telang, 1998). In many Pseudococcinae, T. princeps may in turn host γ-proteobacteria (Candidatus Moranella endobia) that provide essential amino acids for the β-proteobacterium (an interesting tale of genome reduction that is well beyond the scope of this post; López-Madrigal et al., 2015). Polar bodies invade the developing egg, apparently fuse with energids, and are then colonized (Schrader, 1922) by these endosymbiotic bacterial consortia (López-Madrigal et al., 2013), as shown above (von Dohlen et al., 2001).

Diagram of diaspidid life cycle; note triploidy of polar body that undergoes Schrader fusion (Normark, 2004)
Normark (2003) calls such tissues antiplacentas, although this term is somewhat disingenuous. Rather than being extensions of the offspring's zygote that remain within maternal bodies for the remainder of her life, and is indeed essential to the mother's survival, placentas are immediately dispensable things. A comparison to the triploid endosperm of Anthophyta (flowering plants) seems more apt (Gavrilov & Kuznetsova, 2007), as pseudococcid bacteriomes are polyploid due to their origin.

Why the multiple dizygotic systems cited above? And why among the Coccoidea alone does this occur, among all the diversity that is the Metazoa? To be brief, we do not know. Normark (2004) hypothesizes that polar body-based Schrader fusions act to conceal the sex of offspring from endosymbionts, which due to strictly vertical transmission are incentivized to skew sex ratios towards females. In this scenario, Schrader fusion results from genetic conflict between mutualistic symbionts. However, experimental work is required for any substance to attach to this intriguing idea.

*A term for the clade including the Hexapoda, and the "Crustacea" from within which the hexapods descend.
A category into which a confirmed bacterial taxon can be placed pending formal description.
‡Nuclei in a proliferating embryo that have not undergone cleavage, such that they are surrounded by distinct halos of cytoplasm but have no cell walls.


Buchner, P. (1965). Endosymbiosis of Animals with Plant-Like Micro-Organisms. New York: Wiley. 

von Dohlen, C. D.; Kohler, S.; Alsop, S. T.; and McManus, W. R. (2001). Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature, 412, 433-436.

Gardner, A. and Ross, L. (2011). The evolution of hermaphroditism by an infectious male-derived cell lineage: an inclusive-fitness analysis. The American Naturalist, 178(2), 191-201.

Gavrilov, I. A. and Kuznetsova, V. G. (2007). On some terms used in the cytogenetics and reproductive biology of scale insects (Homoptera: Coccinea). Comparative Cytogenetics, 1(2), 169-174.

Haig, D. (1993). The evolution of unusual chromosomal systems in coccoids: extraordinary sex ratios revisited. Evolutionary Biology, 6(1), 69-77.

Hodgson, C. J. and Hardy, N. B. (2013). The phylogeny of the superfamily Coccoidea (Hemiptera: Sternorrhyncha) based on the morphology of extant and extinct macropterous males. Systematic Entomology, 38(4), 794-804.

Hughes-Schrader, S. (1925). Cytology of hermaphroditism in Icerya purchasi (Coccidae). Cell and Tissue Research, 2(2), 264-290.

Hughes-Schrader, S. (1944). A primitive coccid chromosome cycle in Puto sp. The Biological Bulletin, 87(3), 167-176.

Juchault, P. (1999). Hermaphroditism and gonochorism: a new hypothesis on the evolution of sexuality in Crustacea. Comptes Rendus de l'Académie des Sciences - Series III - Sciences de la Vie, 5, 423-427.

López-Madrigal, S.; Balmand, S.; Latorre, A.; Heddi, A.; Moya, A.; and Gil, R. (2013). How Does Tremblaya princeps Get Essential Proteins from Its Nested Partner Moranella endobia in the Mealybug Planoccocus citri? PLOS ONE, 8(10), e77307.

López-Madrigal, S.; Latorre, A.; Moya, A.; and Gil, R. (2015). The link between independent acquisition of intracellular gamma-endosymbionts and concerted evolution in Tremblaya princeps. Frontiers in Microbiology, 6(642), 1-10.

Moran, N. A. and Telang, A. (1998). Bacteriocyte-associated symbionts of insects: a variety of insect groups harbor ancient prokaryotic endosymbionts. BioScience, 48, 295-304.  

Normark, B. B. (2003). The evolution of alternative genetic systems in insects. Annual Review of Entomology, 48, 397-423.

Normark, B. B. (2004). The strange case of the armored scale insect and its bacteriome. PLOS Biology, 2(3), e43.

Ross, L.; Pen, I.; and Shuker, D. M. (2010). Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems. Biological Reviews, 85(4), 807-828.

Ross, L.; Shuker, D. M.; Normark, B. B.; and Pen, I. (2012). The role of endosymbionts in the evolution of haploid-male genetic systems in scale insects (Coccoidea). Ecology and Evolution, 2(5), 1071-1081.

Royer, M. (1975). Hermaphroditism in insects: studies on Icerya purchasi. In Reinboth, R. (ed.): Intersexuality in the Animal Kingdom (pp. 135-145). Berlin: Springer.

Schrader, F. (1922). The sex ratio and oogenesis of Pseudococcus citri. Molecular and General Genetics, 30, 163-182.

Thao, M. L.; Gullan, P. J.; and Baumann, P. (2002). Secondary (γ-Proteobacteria) Endosymbionts Infect the Primary (β-Proteobacteria) Endosymbionts of Mealybugs Multiple Times and Coevolve with Their Host. Applied Environmental Microbiology, 68(7), 3190-3197. 
Tremblay, E. and Caltagirone, L. E. (1973). Fate of polar bodies in insects. Annual Review of Entomology, 18, 421-444. 

Unruh, C. and Gullan, P. (2008). Molecular data reveal convergent reproductive strategies in iceryine scale insects (Hemiptera: Coccoidea: Monophlebidae), allowing the reinterpretation of morphology and a revised generic classification. Systematic Entomology, 33, 8-50.

Friday, December 29, 2017

And Now, Some Shameless Self-Promotion: My First Peer-Reviewed Paper is Out

A sizable chunk of my life, 2015-2017
For the first time, you can read some original research of mine, relating my attempts to find morphometric indices and morphological characters of the soldier caste that could be used to discriminate sympatric species of the pantropical termite genus Heterotermes (Rhinotermitidae: Heterotermitinae). All specimens examined were Puerto Rican, but I hope that these results can be extrapolated to the Caribbean Region at large. Whether or not I was successful in my taxonomic endeavor, those who read this blog regularly (and yes, I know that there are some) might appreciate perusing my first real foray into systematic entomology. 

Yes, it is open-access; I'm not a complete aedeagus.

Tuesday, December 26, 2017

At Long Last, McAlpine's Fly has Got a Name

The adult McAlpine's Fly: B, D, F, and G show female features; the remainder, male (Michelsen & Pape, 2017)
Nearly four decades ago, Ferrar (1979) described the larvae (all instars) and puparia of an undescribed calyptrate fly of uncertain familial assignment, widespread across southern Australia in forested habitats. The paper in question was a survey of dung-feeding Calyptratae (a diverse clade containing some of the most familiar dipterans, from the house fly Musca domestica to the tsetse flies [Glossinidae]) on the Australian continent, and the larvae of this undescribed species were accordingly coprophages reared from cow dung. While visually unassuming, the fly (the first specimens of which were collected by famed Australian dipterist D. K. McAlpine) was noteworthy for two reasons: first, in that it was larviparous (giving live birth), with females brooding single offspring at a time in lecithotrophic* fashion and depositing their larvae directly upon dung; and second, in that the fly could not be readily assigned to any known calyptrate family. While the flies have been reared only from bovine waste, this surely cannot be their original host association given that cows were only introduced to Australia two centuries ago. This is supported by the fact that adults have been collected in Australian habitats from which cows are absent (Michelsen & Pape, 2017).

Ferrar (1979) did not describe the adults, but cited personal communications that they most closely resembled the Anthomyiidae, with male genitalia exhibiting "one or two characters" (Ferrar, 1979) more reminiscent of the Calliphoridae (blowflies), in this sense including both the Rhiniidae and Mesembrinellidae (now each having familial status; Kutty et al., 2010; Marinho et al., 2016). Ferrar (1979) concluded on the basis of both larval biology (sedentary and exclusively dung-feeding) and third-instar larval morphology (radiating slits around posterior spiracles) that "McAlpine's Fly", as it became known, could provisionally be considered an anthomyiid.

Image result for Mystacinobia
Mystacinobia zelandica photographed by Rod Morris
Thereafter, adult specimens were bounced around to multiple fly systematists, each of whom concluded that whatever McAlpine's Fly might be, it was not in their respective taxa of interest (Ferrar, 1987) and thus apparently not worth describing. Nonetheless, its status as a valid taxon was never debated, and McAlpine's Fly was repeatedly referenced in the literature as an enigmatic footnote to fly systematics. The phylogenetic analyses of Kutty et al. (2010), using eight mitochondrial or nuclear loci, convincingly demonstrated (irrespective of model) that McAlpine's Fly was not akin to the Anthomyiidae, but rather a member of the superfamily Oestroidea. Moreover, a biogeographically intriguing sister-group relationship to the uniquely Zealandian, quasisocial bat symbionts of the monotypic Mystacinobiidae (Holloway, 1976) was supported. Kutty et al. (2010) even suggested that the two lone genera could possibly be lumped in the same family, despite their great phenotypic dissimilarity.

Fly - Stevenia deceptoria
Stevenia deceptoria (Rhinophoridae), photographed by John Rosenfeld
After four decades in taxonomic limbo, Michelsen & Pape (2017) have finally deigned to describe adult McAlpine's Flies in detail, under the name Ulurumyia macalpinei. As previously implied by years of placement incertae sedis, U. macalpinei indeed has none of the defining features that could assign it to any calyptrate family. Therefore, these authors establish the Ulurumyiidae for the species. Their description discloses a number of morphological traits that support this taxon's membership in the Oestroidea, although ulurumyiids lack both the distally bent medial vein characteristic of that superfamily (with the exception of some Tachinidae and Rhinophoridae) and a divided female sternite VIII, a character state which in the Oestroidea is only elsewhere encountered in the Mystacinobiidae (Michelsen & Pape, 2017).

While it seems entirely reasonable to place Ulurumyia in its own family, that family's phylogenetic position among the Oestroidea remains a topic of debate. Unpublished transcriptomic data hints not at a sister-group relationship with the Mystacinobiidae, but at kinship with the Calliphoridae sensu lato (Michelsen & Pape, 2017). Specifically, phylogenetic analysis of the Oestroidea suggests with medium to high support (disregarding model) a sister-group relationship between the Ulurumyiidae and Mesembrinellidae (Cerretti et al., 2017). While I do not find these results as compelling as I would like (read the paper), it is interesting that all Mesembrinellidae so far as known also practice larviparity (albeit of the pseudo-placental* variety; Meier et al., 1999).

A very happy Boxing Day to you all.

*Feeding exclusively on egg yolk, with the larva hatching from an egg within its mother. This contrasts with pseudo-placental larviparity, in which case larvae subsist on specialized secretions produced by their mother (Meier et al., 1999). The latter condition is a famed trait of the Hippoboscoidea.
Cooperative brood care among individuals of the same generation, without reproductive division of labor.  
Ventral sclerites of the insect abdomen. Sternites are numbered according to the segment with which they are associated (antero-posterior).

Cerretti, P.; Stireman, J. O.; Pape, T.; O'Hara, J. E.; Marinho, M. A. T.; Rognes, K.; and Grimaldi, D. A. (2017). First fossil of an oestroid fly (Diptera: Calyptratae: Oestroidea) and the dating of oestroid divergences. PLoS One,

Ferrar, P. (1987). A Guide to the Breeding Habits and Immature Stages of Diptera Cyclorrhapha. Entomonograph, 8(1-2). Leiden and Copenhagen: Scandinavian Science Press/E. J. Brill.

Holloway, B. A. (1976). A new bat-fly family from New Zealand (Diptera: Mystacinobiidae). New Zealand Journal of Zoology, 3, 279-301.

Kutty, S. N.; Pape, T.; Wiegmann, B. M.; and Meier, R. (2017). Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidea and the position of Mystacinobiidae and McAlpine’s fly. Systematic Entomology, 35, 614-635.

Marinho, M. A. T.; Wolff, M.; Ramos-Pastrana, Y.; de Azeredo-Espin, A. M. L.; and Amorim, D. S. (2016). The first phylogenetic study of Mesembrinellidae (Diptera: Oestroidea) based on molecular data: clades and congruence with morphological characters. Cladistics, 33(2), 134-152.

Meier, R.; Kotrba, M.; and Ferrar, P. (1999). Ovoviviparity and viviparity in the Diptera. Biological Reviews, 74, 199-258.

Michelsen, V. and Pape, T. (2017). Ulurumyiidae-a new family of calyptrate flies. Systematic Entomology, 42(4), 826-836.

Saturday, October 14, 2017

The Taxonomy Fail Index: a Proposed Modification

In 2010, the ever-prolific ant photographer and notable myrmecologist Alex Wild proposed the Taxonomy Fail Index to quantify error in the identification of organisms. He was inspired by the apparently commonplace idea that cochineal dye is derived from beetles, which, to paraphrase a Krutabulon saying, is total gorgon frass*. Wild proposed the following formula: TFI (Taxonomy Fail Index)=T/H, where T=the period of time since the last common ancestor of organisms A (actual taxon of organism in question) and B (taxon as which the organism in question has been misidentified) lived, and H=period of time since the last common ancestor of humans (Homo sapiens) and chimps (Pan spp.) lived. 

In other words: 
... the Taxonomy Fail Index scales the amount of error in absolute time against the error of misidentifying a human with a chimp. (Wild, 2010)
The periods of time in question are estimated from TimeTree. Of course, these data (compiled from multiple sources) are subject to revision, hence the divergence between Homo and Pan as an anchor: regardless of changes in divergence dating, the error of identifying Sarah Palin as a bonobo (to use Wild's example) will always have a magnitude of 1.0, barring revision to hominid systematics.

The limitation of the TFI, as I see it, is that it provides no means of communicating relative error. The TFI of mistaking a honey bee for a hornet, for example, is 24.4: a number that is uninformative in and of itself. One can contextualize this error's magnitude by saying that it is slightly more stupid than mistaking an opossum for a cat (TFI=23.9), as Alex Wild did, but I would prefer to scale the TFI in some fashion. 

To do so, I calculated the TFI of the most egregious possible Taxonomy Fail: conflating organisms at opposite ends of life's phylogenetic tree. My exemplar was the TFI of identifying Streptococcus sp. as a human being. This comes out to 645.1. The domain Bacteria (Woese et al., 1990) to which Streptococcus belongs is regarded as the sister group of the remaining two domains (Ciccarelli et al., 2006), one of which includes H. sapiens. Theoretically, then, as there is no higher taxonomic rank than that of the domain, 645.1 is the highest possible TFI (barring revision of our notions of life's fundamental phylogeny, which appears improbable at this point). As such, I choose to calibrate the entire Taxonomy Fail Index to the above value. 

Shinkaiya lindsayi (Lecroq et al., 2008), a xenophyophore
One could divide this value by 100, each unit on this Taxonomy Fail Scale being a Wild. Thus, misidentifying any bacterium as any eukaryote or vice versa equals 100 Wilds on the TFS. Therefore, a single Wild equals a TFI magnitude of 645.1/100=6.45. 

With the TFS, we can not only calculate taxonomic error, but provide an inherent comparison between these calculations. To wit: identifying Sarah Palin (or any politician) as a bonobo, or identifying a bonobo as a politician, amounts to 0.155 Wilds on the TFS. For comparison, classifying a xenophyophore (a derived group of gargantuan foraminiferans; Pawlowski et al., 2003) as a sponge (Haeckel, 1889) equals 38.7 Wilds on the the TFS, making this identification one of Ernst Haeckel's more profound mistakes and perhaps the greatest Taxonomy Fail ever to be published under peer review. 

A Megalopyge sp. larva from Peru (Phil Torres), engaging in Muellerian mimicry of Trump's hair
The implications for public discourse are profound: for one thing, misidentifying a megalopygid caterpillar as Donald Trump's hair (18.6 Wilds) is roughly 2 times less erroneous than calling a xenophyophore a sponge.

*A turn of phrase that presupposes gorgons are herbivorous.

Ciccarelli, F. D.; Doerks, T.; von Mering, C.; Creevey, C. J.; Snel, B.; and Bork, P. (2006). Toward Automatic Reconstruction of a Highly Resolved Tree of Life. Science, 311(5765), 1283-1287.

Haeckel, E. (1889). Report on the deep-sea Keratosa. Report on the scientific results of the voyage of H. M. S. Challenger during the years 1873-76. Zoology, 32 (pt. 82), 1-92. 

Lecroq, B.; Gooday, A. J.; Tsuchiya, M.; and Pawlowski, J. (2008). A new genus of xenophyophores (Foraminifera) from Japan Trench: morphological description, molecular
phylogeny and elemental analysis. Zoological Journal of the Linnean Society, 156, 455-464.

Pawlowski, J.; Holzmann, M.; Fahrni, J.; and Richardson, S. L. (2003). Small subunit ribosomal DNA suggests that the xenophyophorean Syringammina corbicula is a foraminiferan. Journal of Eukaryotic Microbiology, 50, 483-487.

Wild, A. (September 9, 2010). The Taxonomy Fail Index. Retrieved 10/13/17 from

Woese, C.; Kandler, O.; and Wheelis, M. L. (1990). Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proceedings of the National Academy of Sciences of the United States of America, 87, 4576-4579. 

Wednesday, September 20, 2017

A "Little Bag of Horror" from the Cretaceous

Of the things that are unlikely to be preserved in the fossil record, the larvae of insects with complete metamorphosis are high on the list. Usually extremely soft-bodied and (it almost goes without saying) small, even their appearance in amber (a medium conducive to the preservation of the small and soft) is rare. An additional taphonomic bias (one that affects the entire fossil record) exists against insect larvae that are not aquatic. So, the description of a fossil larva that is not, say, a Mesozoic fishfly (Corydalidae: Chauliodinae) (of which multiple specimens are known; Liu et al., 2012) is cause for excitement.

Fourth-instar rhopalosomatid larva of unknown genus (Lohrmann & Engel, 2017)
Thus, the news of an indisputable rhopalosomatid larva from Burmese amber (Lohrmann & Engel, 2017) is a cause for excitement. In my case, this is due more to its familial affiliation than its mere identity as an insect larva. You may recall my mention of the Rhopalosomatidae (a small family of aculeate wasps, now one of the two families constituting the Vespoidea sensu stricto) in the inaugural post of Life, et al.: specifically, I drew attention to the oddity of their ectoparasitoid larvae (which, where known, attack crickets [Gryllidae]), which retain multiple instars' worth of molted exuviae, thus forming a protective snakeskin-like sack (Lohrmann & Engel, 2017). This "little bag of horror", as I termed it, was described in detail by Gurney (1953) in the case of Rhopalosoma nearcticum, the egg of which is characteristically placed behind the host's metacoxa, with the larva being positioned thereupon until pupation (see photographs above and below). The cricket host appears to not give that much of a frass about its terminal situation, as mating is unaffected by the presence of the immature parasite (Alexander and Otte, 1967).

The amber inclusion of an unmistakable fourth-instar rhopalosomatid larva, described in situ behind a cricket's hind leg (Gryllidae; it cannot be identified beyond familial level), is a "confluence of rarities" (Lohrmann & Engel, 2017).  Rhopalosomatids are rare in the fossil record, with only four fossil species having been described; of these, only Eorhopalosoma gorgyra from Burmese amber can be confidently assigned to the family (Engel, 2008). (The other three are compression fossils.) Additionally, hosts of the order to which rhopalosomatids' cricket hosts belong (the Orthoptera) are only rarely preserved in amber (Heads, 2009).

View of rhopalosomatid larva's left side and cricket's underside (Lorhmann & Engel, 2017)
The larva's exquisite preservation reveals that it is in all visible respects indistinguishable from the larva of R. nearcticum, as described by Gurney (1953). Since no other rhopalosomatid larvae have been described (Olixon australiae was reared to adulthood but never described as a larva; Perkins, 1908), however, it would be premature to identify it as a member of this New World species.

Regardless of the specimen's generic identity, it is remarkable that rhopalosomatids' niche, and concomitant morphology, has seemingly changed so little in 98 million years. 


Alexander, R. D. and Otte, D. (1967). Cannibalism during copulation of the brown bush cricket, Hapithus agitator (Gryllidae). Florida Entomologist, 50, 79-87.

Branstetter, M. G.; Danforth, B. N.; Pitts, J. P.; Faircloth, B. C.; Ward, P. S.; Buffington, M. L.; Gates, M. W.; Kula, R. R.; and Brady, S. G. (2017). Phylogenomic Insights into the Evolution of Stinging Wasps and the Origins of Ants and Bees. Current Biology, 27(7), 1019-1025. DOI:

Engel, M. S. (2008). The wasp family Rhopalosomatidae in mid-Cretaceous amber from Myanmar (Hymenoptera: Vespoidea). Journal of the Kansas Entomological Society, 81, 168-164.

Gurney, A. B. (1953). Notes on the biology and immature stages of a cricket parasite of the genus Rhopalosoma. Proceedings of the United States National Museum, 103, 19-34.

Heads, S. W. (2009). A new pygmy mole cricket in Cretaceous amber from Burma (Orthoptera: Tridactylidae). Denisia, 26, 75-82.

Liu, X.; Wang, Y.; Shih, C.; Ren, D.; and Yang, D. (2012). Early Evolution and Historical Biogeography of Fishflies (Megaloptera: Chauliodinae): Implications from a Phylogeny Combining Fossil and Extant Taxa. PLoS One, 7(7), e40345. Retrieved 9/17/17 from

Lorhmann, V. and Engel, M. S. (2017). The wasp larva's last supper: 100 million years of evolutionary stasis in the larval development of rhopalosomatid wasps. Fossil Record, 20, 239-244. Retrieved 9/16/17 from

Perkins, R. C. L. (1908). Some remarkable Australian Hymenoptera. Proceedings of the Hawaiian Entomological Society, 2, 27-35. 

Thursday, July 27, 2017

Three New Orders of Insecta in Burmese Amber: is this Really Necessary?
Prokoenenia wheeleri (Palpigradi: Prokoeneniidae) from Texas; attribution shown
For the past two decades, the amber deposits of the Hukawng Valley in Myanmar's Kachin State have been intensely scrutinized by paleoentomologists. The burmite recovered from this locale dates to the very end of the Cenomanian Stage (98.79 mya; Shi et al., 2012). Containing everything from what is by far the oldest known specimen of the flagrantly obscure arachnid order Palpigradi (largely the same as its modern counterparts; Engel et al., 2016) to uniquely specialized haidomyrmecine ants (weirdly unlike any of their modern counterparts; Perrichot et al., 2016), it is a treasure trove of exquisite Cretaceous microfaunal data.

Just within the past year and a half, three (count 'em, three) new insect orders have been described from Hukawng Valley burmite: namely, the Alienoptera (Bai et al., 2017), Aethiocarenodea (Poinar & Brown, 2017), and Tarachoptera (Mey et al., 2017). (And this is not even to mention the Permopsocida, an order that was established for Permian-Cretaceous insect taxa after the description of a specimen from the Hukawng Valley; Huang et al., 2016). After we pick our collective mandibles up off the floor, we should consider each of these taxa in turn: are their ordinal statuses truly defensible? Or, perhaps, are these better regarded as stem-groups of extant taxa?

Kinitocelis divisinotata, holotype (adult female)
First off, the Tarachoptera. This order consists of two genera, both placed in the Tarachocelidae. This peculiar family is clearly a member of the superorder Amphiesmenoptera, a clade consisting of the extant orders Lepidoptera (moths, and the diurnal moths we call "butterflies") and Trichoptera (caddisflies); of the 14 autapomorphic* amphiesmenopteran characters listed by Kristensen (1984) that are applicable to adult amber inclusions, only 3 are incontrovertibly absent from the Tarachocelidae (for what it's worth, paired setose pronotal warts, setose sclerites below or behind the metathoracic subalare, and rod-like apodemes on the eighth and ninth female abdominal segments; Mey et al., 2017).

Wing scales of Kinitocelis brevicostata (Tarachoptera: Tarachocelidae)
However, the unassuming, mandibulate-moth-like tarachocelids cannot be placed in either extant order of the Amphiesmenoptera. They possess scales on their wings, reminding one of the Lepidoptera; but this resemblance appears to be a superficial convergence, as some trichopterans have developed scale independently of their origin in the Lepidoptera (Huxley & Barnard, 1988)—meaning that it is plausible that scales could emerge independently as well in the Tarachocelidae (Mey et al., 2017). Conversely, the specialized haustellum (proboscis) and single nygma on the forewing characteristic of the Trichoptera are conspicuously lacking in all examined tarachocelid specimens (Mey et al., 2017). 

Head profiles of basal trichopterans and lepidopterans (23-24) and K. brevicostata (Tarachoptera; 25)
In short, not only can the Tarachocelidae not be placed in any extant order, but they also cannot be incontrovertibly judged more closely related to either of the extant amphiesmenopteran orders than to the other. One could say that the Tarachoptera are like what the most primitive Amphiesmenoptera would have been, were it not for some peculiar derived traits of their own: among these are vestigial maxillary palpi (quite unlike the functional examples in the basalmost moths and caddisflies—see above); a single medial wing vein (otherwise known from insects only in the monotypic glossatan moth family Aenigmatineidae, thus far described only from Australia's Kangaroo Island; Kristensen et al., 2014); and the absence of tibial spurs, which with the exception of a few odd lepidopterans are a universal feature of insects with complete metamorphosis. Since tibial spurs are involved in launching adult insects into flight (Burrows & Durosenko, 2015), tarachocelids' lack of them suggests that their flying capability was limited.

While eccentric autapomorphies juxtaposed with basal traits amount to a syndrome typical of stem-groups all across the tree of life, the fact that one cannot argue that Tarachocelidae is more closely akin to either the Trichoptera or Lepidoptera leads me to agree that one could parsimoniously grant the Tarachoptera ordinal rank. However, whether this is necessary is another question.

Type specimen of Aethiocarenus burmanicus
Unlike the Tarachoptera, the Aethiocarenodea were described based on a single species, Aethiocarenus burmanicus. A. burmanicus is known from a single adult female specimen, and is like nothing else on Earth: a small, wingless, flattened insect, with a narrow corpus and a triangular head with its hypotenuse situated opposite to its articulation with the thorax—a condition quite unlike the head of any other insect, extant or otherwise. The head is strongly hypognathous§ (see below), making for a distinctive profile. Adding an additional memorable trait to this already memorable habitus, a pair of apparently secretory glands were situated on the back of the neck (presumably defensive in function) (Poinar & Brown, 2017).

Profile of A. burmanicus holotype head
What do we make of this creature, taxonomically speaking? Very little, judging from Poinar & Brown (2017), who do not speculate on its phylogeny nor even bother to assign it provisionally to any subdivision of the Insecta. The presence of cerci would exclude it from the clade Acercaria (Hemiptera, Psocodea, etc.; Huang et al., 2016) and from those insect superorders that practice complete metamorphosis (e.g., the Amphiesmenoptera), leaving the only possible assignment for the Aethiocarenodea as the Polyneoptera. This assemblage may or may not be monophyletic (Beutel et al., 2013), and there is little basis for direct comparison of the Aethiocarenodea with its fellow members; all fourth tarsomeres extend distally beneath the respective fifth tarsomeres, which Poinar & Brown (2017) note vaguely recalls the tarsal condition of some Dermaptera (earwigs). We thus remain at a loss for valid comparisons to situate the Aethiocarenodea in the insect family tree. However, as argued by Christopher Taylor (rather more eloquently than I could put it), this does not necessarily warrant ordinal status: to place A. burmanicus in its own order is more an admission of ignorance than anything else.

By contrast, the (again monotypic) Alienoptera are clearly akin to mantises (Mantodea). Described from a single male specimen of Alienopterus brachyelytrus (Bai et al., 2016), the taxon is a creature with a triangular head and bristly profemora not unlike those of the most ancient mantids. While most of the features that define the Dictyoptera (cockroaches, termites, and mantises) cannot be falsified on the specimen of A. brachyelytrus, the presence of a profemoral brush (otherwise unique to the Mantodea) and excellently preserved genitalia clinch its classification therein.

Alienopterus brachyelytrus: enlarged arolia, tegmina, and orthognathous head are all visible
The Alienoptera can be distinguished from the Mantodea mainly on the basis of two peculiar characters: greatly shortened, sclerotized forewings analogous to those for which the Dermaptera are named, and utterly unlike anything observed in any Mantodea; and enlarged arolia|| reminiscent of those exhibited by the rockcrawlers (Mantophasmatodea) (Beutel & Gorb, 2008). Mantises, conversely, lack arolia (with the possible exception of the extinct Santanmantis). More conspicuously, the Alienoptera do not have the raptorial forelegs for which all mantises living and extinct are known (Wieland, 2013); the vestiture of the profemora would not have worked in opposition to tibial spines as it would in mantises' case.

Most of these traits are "retained ancestral conditions", since the ancestral dictyopteran presumably also lacked protibial spines and retained arolia; the "array of specialized [alienopteran] features" (autapomorphies, to use phylogenetic jargon) consist only of a saddle-shaped pronotum and earwig-like tegmina. Bai et al. (2016) exclude the species from the Mantodea proper, and reasonably so, but does this justify erecting a new order for the taxon?

In my opinion, no. To begin with, a strict consensus tree using 58 morphological characters firmly placed Al. brachyelytrus as the sister group to the Mantodea (Bai et al., 2016). Even the 30% of this male specimen's genitalia that is visible, a suite of body parts that Bai et al. (2016) duly note have evolutionary plasticity to a degree that they may differ even within the same order (Klass, 1997), "fully conform to the condition within" mantises. Moreover, the characters that exclude Al. brachyelytrus from the Mantodea are mostly "retained ancestral conditions", making this mantodean sister-group not a mantis by dint of lacking derived mantodean traits.  

Al. brachelytrus is as such not excluded from the Mantodea because it has closer kin elsewhere, but because it lacks some (but not all) of the derived traits that define that order: the status of the Alienoptera is thus contingent upon how broadly one wishes to spread the definition of the Mantodea. The bounds of that definitionwhere a basal dictyopteran more closely related to mantises than to any other extant taxon becomes itself a "mantis"are subjective.
Nymph and adult of Cryptocercus punctulatus (Cryptocercidae); photograph by David R. Maddison
For comparison, consider the cockroach family Cryptocercidae. Being subsocial wood-feeders dependent upon oxymonadids and hypermastigids in their hindguts for cellulose digestion, these cockroaches bear an obvious biological and morphological resemblance to termites, and are regarded as the sister-group of the infraorder Isoptera (Engel et al., 2009). With the exception of adult winglessness (an apomorphy), the features that distinguish the Cryptocercidae from termites are basal conditions with respect to the Isoptera: e.g., an ootheca (egg-case; vestigial or absent in termites). One could simply say, therefore, that cryptocercids are stem-group termites: we only call them "cockroaches" due to the convenience of that term. Likewise, one can either refer to Alienoptera as a mantodean stem-group, or as its own order. Arguably, neither position is "false", and so ordinal ranking is a matter of preference: of whether one chooses to lump or to split. And I, personally, would advocate that personal preference does not a new order make.
Bornean Metallyticus splendidus (Metallyticidae); photographed by Paul
On a tangent, given the clear anatomical gulf between cryptocercids and even the most basal known termite (Cratomastotermes wolfschwenningeri, a mid-Cretaceous Brazilian specimen classified in its own family; Engel et al, 2009), one could argue that an analogy between this systematic situation and that of the Alienoptera with respect to the Mantodea is stretching things a bit. However, given that the ancestral ethological condition of the Mantodea was that of prowlers on or under bark (Wieland, 2010; the metallyticid shown retains this basal niche), unlike the clearly foliage-abiding Al. brachyelytrus (Bai et al., 2016), there certainly was an ecological distinction between that insect and contemporary mantises.

In conclusion, I think that of the Alienoptera, Aethiocarenodea, and Tarachoptera, only the latter order is truly deserving of that rank, given the information now available. However, I admit that further data could lend support to the Aethiocarenodea: I think that a comprehensive search of other Cretaceous ambers for kin to this enigmatic little creature is in order. 

*A derived trait unique to a particular taxon.
A sclerite immediately adjacent to the base of the insect wing, providing a place of attachment to the pleural wing muscle.
Ingrowths of the exoskeleton, serving as attachments for muscles.
§With downward-directed mandibles.
||An unsegmented lobe extending from the tip of the insect tarsus, situated between the tarsal claws.
A derived trait (with reference to its ancestral state) in a particular taxon, but not one necessarily unique to that taxon.

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