Fossil Insect Parasitism

One question we palaeontologists get more often than we should is how we can show behaviour in the fossil record. The answer is simple: for most behaviour, we can’t show any direct evidence. If the behaviour results in a modification of the environment, then those traces can be found as trace fossils (ichnofossils), which are the subject of their own subdiscipline of palaeontology. Besides burrows and footprints, bite marks and drill holes show predation on vertebrates and shelly animals, and plant fossils can show many signs of insect feeding and oviposition. All of these can be compared to modern counterparts to get remarkably precise identifications of the culprits.

I’ve been asked specifically about parasitic behaviour, and more specifically about entomology, so here is a quick review of sorts of palaeontomological parasitism. You can read the link above for fossil galls (insects parasitising plants), the rest of this article will be animal-on-animal action.

First off, it must be admitted that parasites are among the smallest and softest animals, so they’re not exactly common as fossils. The point of this post is to show that this standard warning, while true, is too often too hastily applied. The fossil record has many surprises and much more information than it’s commonly given credit for.

Most parasitic behaviours require specific anatomical adaptations to carry out, and these can also be found in fossils. The organisms whose anatomy changes the most due to behaviour are parasites, and through the fossil record we can trace the evolution of these specialised anatomies, and thereby get a finer view of their transition to parasitism.

For example, the Hymenoptera are most well-known as bees, wasps, and ants, but the bulk of their diversity is contained in a great array of parasites and parasitoids. One parasitic superfamily is the Chalcidoidea, most of whose larvae are parasites of other insects and spiders. The species we know from amber (see e.g. Arillo & Ortuño, 2005) will most likely also be parasites.

quasicimex

The same can be said for Quasicimex eilapinastes above, a stem-group cimicid (bed bugs and relatives) described by Engel (2008). Just by virtue of its phylogenetic position, a null hypothesis of parasitism is the most warranted.

Often, you’ll find that the fossil contains a lot of information if you know what to look for. In hymenopterans, the parasitoid way of life is enabled by an elongated ovipositor, which can be seen in hymenopteran fossils as early as the mid-Jurassic (see Donald Quicke’s 1997 Parasitic Wasps), so we know that this was an early innovation and we can make a reasonable argument that these early specimens were, in fact, also parasitoids.

athericid

This kind of inference is the most common way of deciphering fossil behaviour, and it depends on the preservation of the fossil, its phylogenetic position, and a bit of grounded imagination. Take the very recent find of a fossil aquatic athericid fly larva by Chen et al. (2014). Alongside specialised bristles, Qiyia jurassica had piercing mouthparts and unique suckers instead of legs, which functioned much like octopus suckers and could anchor it on a host. Coupled with the fact that it could not have moved its head much, a very likely lifestyle is as an ectoparasite, the authors speculating salamanders as hosts. This interpretation can be contested, but the evidence for it is very good, despite us not seeing it sucking on any animal.

strep_ct

I can hear the cries already: “Most fossils are too badly-preserved to get such fine details!” To anyone shouting this, first, let me welcome you to the 21st century. Would you like some juice to help you get over the time-travelling-jet-lag? Then, look up at that picture. Looks like a typical µCT reconstruction of a strepsipteran, the weirdest parasitic insects. Except that the specimen in this case is a strepsipteran from Baltic amber (Pohl et al., 2010). You can see all the internal and external anatomical details that may or may not be involved in their parasitism.

huang2014

Diying Huang recently reviewed our knowledge of Mesozoic giant fleas, examples and reconstruction pictured above, whose morphologies show similar adaptations to ectoparasitism as modern fleas, and were most likely parasitising early mammals and perhaps even some dinosaurs. Our anatomical resolution is high enough that we can discount pterosaurs as potential hosts: modern fleas that parasitise bats have specialised “hooks” to avoid being thrown off the wing during flight; none of the Mesozoic fleas have those. Note that there is still debate as to whether these are “true” fleas or not, as the phylogeny by Zhu et al. (2015) shows the earliest fleas as being of Cretaceous age, younger than the mega-fleas. Regardless, the mega-fleas are somewhere in the stem-group, and if anything, they show the basalness of parasitism in fleas.

Younger and definite fleas from Dominican and Baltic ambers (see Footnote 1) are so similar to their modern counterparts that they fall in the same genera. We may not see them sucking on any blood, but we can be 99.9% sure these critters were parasites.

In 2013, Greenwalt et al. published a study showing the presence of heme (the main component of vertebrate blood) in the abdomen of a rock-preserved mosquito from the 46 Ma Kisheneh Formation in Montana, USA. The mosquito may be fossilised by itself without a host, but that heme could only come from the mosquito having an identical parasitic lifestyle to modern mosquitoes. A chemical analysis was done in 2014 by Yao et al. for fossil heteropterans from the Yixian Formation, China. These are relatives of bed bugs and assassin bugs, and the analyses confirm that they are indeed blood-feeding insects: the insect bodies were full of iron, whereas the rock matrix had only trace amounts. Insect blood does not have haemoglobin, therefore all the iron must come from feeding.

wappleretal2004

If you don’t trust the mass-spectrometers that got those results, then you can also find direct remnants of the host in the fossil, as Wappler et al. (2004) discovered in their fossil louse from the Eckfeld Maar, Germany. This was the very first fossil louse ever found, and it came free with remains of bird feathers in its gut. In the picture above, it’s on the left and a modern louse on the right.

engel2005

If all that is still too much inference for your tastes, sometimes you can even see the parasitism in action. Case in point: Engel (2005) describes the highly-specialised triungulin larva of a meloid beetle grabbing onto bee hairs… in Baltic amber, just like we would see them in a field today.

acrocerid

The image above shows a spectacular case of a larval acrocerid fly parasitising an anystid mite. Such an interaction was first described by Sferra (1986) in extant specimens, but the report was widely dismissed, until it was vindicated by this Baltic amber specimen described by Peter Kerr and Shaun Winterton in 2008. It’s an exceptional case, but it just goes to show how surprisingly awesome the fossil record can be.

The strepsipteran fossil record isn’t restricted to the amazing µCT species I mentioned a few paragraphs above. Pohl & Kinzelbach (2001) describe a clearly stylopised Baltic amber ant. That’s as direct evidence of parasitism as you could wish for.

laelapidae

Sometimes, the visual is stunningly clear but we cannot make a clear interpretation. The above picture is from a Baltic amber specimen showing a mite attached to an ant’s head (Dunlop et al., 2014). The mite is from the Laelapidae family, a modern myrmecophilous family, so we can reliably infer that this fossil isn’t just a coincidental occurrence, but it’s not really possible to say with certainty whether the mite is a phoretic parasite or if it’s attacking the ant.

img152

Sometimes we have a classic case of TMI on our hands, as in the main diagram on the slide above. The diagram comes from Eichmann (2003), and as you can see from my helpful arrows, it shows two flies from different families having sex with each other. Not only that, if you look at the chironomid‘s abdomen, you can see that it’s got quite a bulge. Finally, check out its antennae: even though this is a male chironomid, those antennae are slender female antennae, not bushy male antennae. This mix of characters is known from modern chiironomids when they are parasitised by mermithid nematodes. Even though we cannot see any parasites in this specimen, it is clear that they’re there.

There are plenty more examples of insects as victims of parasites. Fungi are one of the most prominent parasites and pathogens of fossils, and we have two awesome fossils showing the antiquity of such relationships.

cordyceps1

Direct evidence comes courtesy of Sung et al. (2008), who describe a Burmese amber male scale insect with an Ophiocordyceps relative sticking out of its head, seen above.

cordyceps2

You might remember Ophiocordyceps as the “zombifying fungus” that controls the brains of ants and other insects, getting them to die in exactly the right place for the fungal spores to spread. In the case of ants, Ophiocordyceps manipulates the ant to go to the underside of a leaf and bite down hard into a vein so the body gets anchored. Obviously, this leaves a scar on the leaf… and Hughes et al. (2011) found that precise scar in a 48Ma leaf from Messel, Germany, which you can see above (a-e are the fossil, f-i are modern comparisons).

Less spectacular infections can be found as well, of course. Way back in 1984, an infected ant was described from Dominican amber by Poinar & Thomas. Mites can be found on two moths in the Dominican amber (Poinar et al., 1991). George Poinar described many pieces of amber showing nematodes popping out of insect bodies, summarised in a review paper.

streblid-plasmod

Let’s not forget that insects are not just parasites and victims of parasites, they can also be neutral vectors. The work of George Poinar Jr. on fossil parasites, and especially amber insects and the trypanosomatids and plasmodiids they carry, is amazing. I have listed some cool papers in footnote 2. The picture above shows two oocysts of a plasmodiid on a streblid fly, from Poinar (2011).

Besides the antiquity of parasitic interactions and the evolution of parasitism in individual lineages, the presence of all these interactions also allows us to infer the potential unpreserved biodiversity. We know that modern evaniid wasps are specialised for parasitising cockroaches, so if we find a fossil one in a locality, we can make a reasonable case that cockroaches were also part of that ecosystem. The other possibility is that the shift to exclusive cockroach parasitism was more recent than the hypothetical fossil, in which case the fossil wasp can provide precious details on that transition.

Finally, one last bit of information that can be acquired is biogeographical. Tsetse flies are nowadays restricted to the Sahel region and parts of the Middle East, but specimens from the Florissant Shale of Colorado (Cockerell, 1918) prove that tsetse flies were once parasitising vertebrates in the Americas too.

Footnotes:

1: The species I refer to here are the Baltic amber Palaeopsylla klebsiana (Dampf, 1910), P. dissimilis (Peus, 1968), P. baltica (Beaucournu & Wunderlich, 2001), P. groehni (Beaucournu, 2003), and the Dominican amber Pulex larimerius (Lewis & Grimaldi, 1997).

2: Plasmodiids: with biting midge (Poinar & Telford, 2005), with mosquito (Poinar, 2005a), with bat flies (Poinar, 2011); Trypanosomatids: with biting midge (Poinar, 2008a), with sand fly (Poinar, 2008b), with assassing bug (Poinar, 2005b).

Further Reading:

Arillo AGA. 2007. Paleoethology: fossilized behaviours in amber. Geologica Acta 5, 159-166.

Labandeira CC. 2002. Paleobiology of predators, parasitoids, and parasites: death and accomodation in the fossil record of continental invertebrates. Paleontological Society Papers 8.

References:

Arillo AGA & Ortuño VM. 2005. Catalogue of fossil insect species described from Dominican amber (Miocene). Stuttgarter Beiträge zur Naturkunde B 352.

Beaucournu JC & Wunderlich J. 2001. A third species of Palaeopsylla Wagner, 1903, from Baltic amber (Siphonaptera: Ctenophthalmidae). Entomologische Zeitschrift 111, 296-298.

Beaucournu JC. 2003. Palaeopsylla groehni n. sp., quatrième espèce de puce connue de l’ambre de la Baltique (Siphonaptera, Ctenophthalmidae. Bull. Soc. Ent. France 108, 217-220.

Chen J, Wang B, Engel MS, Wappler T, Jarzembowski EA, Zhang H, Wang X, Zheng X & Rust J. 2014. Extreme adaptations for aquatic ectoparasitism in a Jurassic fly larva. eLife 3, e02844.

Cockerell TDA. New species of North American fossil beetles, cockroaches and tsetse flies. Proceedings of the US National Museum 54, 301-311.

Dampf A. 1910. Palaeopsylla klebsiana n. sp. Ein fossiler Floh aus dem baltischen Bernstein. Schriften der Physikalisch-Ökonomischen Gesellschaft zu Königsberg, 248.

Dunlop JA, Kontschán J, Walter DE & Perrichot V. 2014. An ant-associated mesostigmatid mite in Baltic amber. Biology Letters 10, 20140531.

Eichmann, F. 2003. Aus dem Leben im Bernsteinwald. Arbeitskreis Paläontologie Hannover 31, 89-94

Engel MS. 2008. A stem-group cimicid in mid-Cretaceous amber from Myanmar (Hemiptera: Cimicoidea). Alavesia 2, 233-237.

Engel MS. 2005. An Eocene ectoparasite of bees: The oldest definitive record of phoretic meloid triungulins (Coleoptera: Meloidae; Hymenoptera: Megachilidae). Acta Zoologica Cracovensia B 1-2, 43-48.

Greenwalt DE, Goreva YS, Siljeström SM, Rose T & Harbach RE. 2013. Hemoglobin-derived porphyrins preserved in a Middle Eocene blood-engorged mosquito. PNAS 110, 18496-18500.

Huang D. 2014. The diversity and host associations of Mesozoic giant fleas. National Science Review 1, 496-497.

Hughes DP, Wappler T & Labandeira CC. 2011. Ancient death-grip leaf scars reveal ant–fungal parasitism. Biology Letters 7, 67-70.

Kerr PH & Winterton SL. 2008. Do parasitic flies attack mites? Evidence in Baltic amber. Biological Journal of the Linnean Society 93, 9-13.

Lewis RE & Grimaldi DA. 1997. A pulicid flea in Miocene amber from the Dominican Republic –(Insecta, Siphonaptera, Pulicidae). American Museum Novitates 3205.

Liu Z, Engel MS & Grimaldi DA. 2007. Phylogeny and geological history of the cynipoid wasps (Hymenoptera, Cynipoidea). American Museum Novitates 3583.

Peus F. 1968. Über die beiden Bernstein-Flöhe (Insecta, Siphonaptera). Paläontologische Zeitschrift 42, 62-72.

Pohl H & Kinzelbach R. 2001. First record of a female stylopid (Strepsiptera: ?Myrmecolacidae) parasite of a prionomyrmecine ant (Hymenoptera: Formicidae) in Baltic amber. Insect Systematics & Evolution 32, 143-146.

Poinar GO. 2003. Trends in the Evolution of Insect Parasitism by Nematodes as Inferred from Fossil Evidence. The Journal of Nematology 35, 129-132.

Poinar GO. 2005a. Plasmodium dominicana n. sp. (Plasmodiidae: Haemospororida) from Tertiary Dominican amber. Systematic Parasitology 61, 47-52.

Poinar GO. 2005b. Triatoma dominicana sp. n. (Hemiptera: Reduviidae: Triatominae), and Trypanosoma antiquus sp. n. (Stercoraria: Trypanosomatidae), the First Fossil Evidence of a Triatomine-Trypanosomatid Vector Association. Vector-Borne and Zoonotic Diseases 5, 72-81.

Poinar GO. 2008a. Leptoconops nosopheris sp. n. (Diptera: Ceratopogonidae) and Paleotrypanosoma burmanicus gen. n., sp. n. (Kinetoplastida: Trypanosomatidae), a biting midge – trypanosome vector association from the Early Cretaceous. Memórias do Instituto Oswaldo Cruz 103, 468-471.

Poinar GO. 2008b. Lutzomyia adiketis sp. n. (Diptera: Phlebotomidae), a vector of Paleoleishmania neotropicum sp. n. (Kinetoplastida: Trypanosomatidae) in Dominican amber. Parasites & Vectors 1, 22.

Poinar GO. 2011. Vetufebrus ovatus n. gen., n. sp. (Haemospororida: Plasmodiidae) vectored by a streblid bat fly (Diptera: Streblidae) in Dominican amber. Parasites & Vectors 4, 229.

Poinar GO & Thomas GM. 1984. A fossil entomogenous fungus from Dominican amber. Experientia 40, 578-579.

Poinar GO & Telford SR. 2005. Paleohaemoproteus burmacis gen. n., sp. n. (Haemospororida: Plasmodiidae) from an Early Cretaceous biting midge (Diptera: Ceratopogonidae). Parasitology 131, 79-84.

Poinar GO, Treat AE & Southcott RV. 1991. Mite parasitism of moths: Examples of paleosymbiosis in Dominican amber. Experientia 47, 210-212.

Pohl H, Wipfler B, Grimaldi D, Beckmann F & Beutel RG. 2010. Reconstructing the anatomy of the 42-million-year-old fossil †Mengea tertiaria (Insecta, Strepsiptera). Naturwissenschaften 97, 855-859.

Sferra NJ. 1986. First record of Pterodontia flavipes (Diptera: Acroceridae) larvae in the mites Podothrombium (Acari: Trombidiidae) and Abrolophus (Acari: Erythraeidae). Entomological News 97, 121-123.

Sung G-H, Poinar G & Spatafora JW. 2008. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses. Molecular Phylogenetics and Evoluton 49, 495-502.

Wappler T, Smith VS & Dalgleish RC. 2004Scratching an ancient itch: an Eocene bird louse fossilProc. R. Soc. B 271 (Suppl. 5), S255-S258.

Yao Y, Cai W, Xu X, Shih C, Engel MS, Zheng X, Zhao Y, Ren D. 2014. Blood-Feeding True Bugs in the Early Cretaceous. Current Biology 24, 1786-1792.

Zhu Q, Hastriter MW, Whiting MF & Dittmar K. 2015. Fleas (Siphonaptera) are Cretaceous, and evolved with Theria. Molecular Phylogenetics and Evolution 90, 129-139.

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