Aphids: The Evolution…

Hello again! In the last post we discussed some of the research regarding aphid origins and paleontology, as well as some of the questions that Heie (2009) wanted answering. We briefly covered one of the main influences on aphid evolution – the host plants. In this post I’ll be discussing some of the key points about host plants in regards to aphid evolution and also some interesting things about their unique morphology.

Sit back, close your eyes and imagine you have traveled back to a time where magnificent dinosaurs rule the earth. However, despite what most children’s shows and textbooks will tell you, dinosaurs aren’t the only animals roaming here. Also, don’t close your eyes for too long, the impact of a written article is diminished if it isn’t actually read.

jurassic-aphid

*Photo Credit: Julian Beniers “Clever Girl” (Not the right scene but hey-ho!)

Interactions between insects and their plant hosts can be considered to be very sensitive. This relationship has been used to investigate the evolutionary histories of many insect species, including the aphids. There are two main theories as to how this relationship may have affected the evolution of both parties;

  • Cospeciation
  • Speciation via the changing of hosts

The first theory eludes to the evolution of both insect and host at the same time, resulting in similar phylogenetic trees. The second refers to the ‘host parasite’ changing its host a number of times, resulting in a literal change in the characteristics of the host parasite.

Although some aphids aren’t necessarily picky with their choice of host plant, many are still considered to have very specific relationships with them. This can be seen when comparing the diversity of some plant species with the aphids that colonise them. The Compositae (around 19,000 sp.) host over 600 species of aphids, which is similar in number to many other plant groups. This can be compared to other groups such as the Coniferae (around 400 sp.) which hosts around 363 species of aphid. Aphids during the later geographical periods would have originally fed upon ancient gymnosperms as angiosperms had not occurred prior to the Cretaceous. However, the evolution and diversification of flowering plants is often regarded as the defining factor that drove aphid evolution which resulted in the aphids that we see today.

geo-plant-ts

* Geographical Time Scale and Plant Evolution

Another factor that will have affected evolution is that of the aphid life cycles. Aphids are divided into non-host alternating (Autoecious), or host alternating (Heteroecious).

Host alternation is a strategy only adapted in around 10% of aphid species but is thought to have significantly contributed towards the colonisation of a wider range of plants and thus has partially driven the evolution of the aphids. A large number of aphids specialise and only feed on one or a few species of plants, whereas host alternation usually occurs seasonally between a woody winter host plant and a secondary summer host that is usually an herbaceous plant species. This constant shift between hosts may have been a deciding factor for the speciation of some aphids prior to present day taxonomy.

life-cycle

*A) Life cycle of the sycamore aphid, Drepanosiphum platanoidis (Autoecious). B) Life cycle of the bird cherry-oat aphid, Rhopalosiphum padi (Heteroecious).

The Aphididae is made up of around 5000 species. The super family Aphidoidea can be considered as aphids which possess siphunculi or siphuncular pores, which would not have been present in most aphid families that existed prior to or during the Cretaceous. One of the questions Heie asks is “where does the family Lachnidae belong on the phylogenetic tree?” I won’t go too much into aphid Phylogenetics because it would need several posts of its own to even begin to cover it in enough detail. So this will be a very brief overview, which I will return to in more detail in future posts.

Aphids of the family Lachnidae are generally brownish in colour, covered in a dense layer of hairs or setae and are (in most species) ‘farmed’ by ants. The oldest known fossils of this family date to the middle Tertiary and are thought to have originated from temperate regions in the Northern hemisphere. The Lachnidae have been through many changes in their taxonomy through the years (see the table below for a brief history!) but in 2015 a paper was published with some updated information on this group of aphids.

Taxonomist Date of Literature Taxonomy
BURMEISTER, 1835 Koch, 1854 Genus – Lachnus
HERRICH-SCHAEFFER Koch, 1857 Family – Lachnidae
Baker, 1920 Lachnidae = Tribe within Aphidinae
Börner, 1952. Heie, 1980 Family – Lachnidae

So are the Lachnidae a primitive group of aphids or a relatively young group in the world of aphid phylogeny? Older (pre-1960’s) literature regarded the Lachnidae as one of the more primitive groups of aphids, but Heie (along with others) disputed this, saying that they are in fact one of the more recent divergences. This may be due to a lack of diversity within the Lachnidae up to the later Tertiary compared to its diversity today. Based on morphology, the Lachnidae have also been considered as the sister group of the Aphididae due to similarities in the presence of wax glands, the oval secondary rhinaria and because some species appear to be morphologically similar.

Molecular studies on this family have also found some contradiction in the evolutionary history of the Lachnidae. One study (see Ortiz-Rivas & Martinez-Torres, 2010) looking at a range of aphid species discovered that the Lachnidae are only distantly related to the Aphididae and that they represent one of the earlier branches in aphid phylogenetic history. The other study (see Novàkovà et al. 2013) utilises the aphid symbiont Buchnera and found that the Lachnidae may be the sister group of the Drepanosiphidae, so may originate from a branch in aphid phylogenetics that is very distant from the branch of the Aphididae. The latter results may be due to mutations in Buchnera or cross contamination between individuals over time.

So it seems as if this topic is still up to some debate between the researchers! See Heie, 2015 in the references below for a more thorough examination of this topic 🙂

Aphids: The Evolution Part 2 – Morphology will be released at the beginning of April (once my coursework exams are all finished!). I hope you enjoyed reading, leave me a comment if you have any questions or suggestions!

I hope to see you again soon 🙂

Picture References

“Clever Girl” by Julian Beniers. Background: http://www.geocities.ws/jp_dinosaurs/compy.html Aphid: https://nl.pinterest.com/kingpiratedog/aphids/

Geographic Time Scale (plant): from https://www.britannica.com/science/Mesozoic-Era

Life cycle image: from http://what-when-how.com/insects/sternorrhyncha-jumping-plant-lice-whiteflies-aphids-and-scale-insects/

References

Dixon, A.F. and Kundu, R.A.N.A.J.I.T., 1994. Ecology of host alternation in aphids. European Journal of Entomology. 91(1), pp.63-70.

Heie, O.E. 2015. A theory about the evolutionary history of Lachnidae and comments on the results of some molecular phylogenetic studies of aphids (Hemiptera: Aphidoidea). Polish Journal of Entomology. 84, pp.275-287.

Huang, X.L., Xiang‐Yu, J.G., Ren, S.S., Zhang, R.L., Zhang, Y.P. and Qiao, G.X. 2012. Molecular phylogeny and divergence times of Hormaphidinae (Hemiptera: Aphididae) indicate Late Cretaceous tribal diversification. Zoological journal of the Linnean Society. 165(1), pp.73-87.

Kim, H., Lee, S. and Jang, Y. 2011. Macroevolutionary patterns in the Aphidini aphids (Hemiptera: Aphididae): diversification, host association, and biogeographic origins. Plos One. 6(9), p.e24749.

Labandeira, C.C. and Phillips, T.L. 1996. Insect fluid-feeding on Upper Pennsylvanian tree ferns (Palaeodictyoptera, Marattiales) and the early history of the piercing-and-sucking functional feeding group. Annals of the Entomological Society of America, 89(2), pp.157-183.

Moran, N.A., Kaplan, M.E., Gelsey, M.J., Murphy, T.G. & Scholes, E.A. (1999). Phylogenetics and evolution of the aphid genus Uroleucon based on mitochondrial and nuclear DNA sequences. Systematic Entomology. 24, pp.85-93.

Novàkovà E., Hypša V., Klein J., Foottit R.G., Von Dohlen C.D. and Moran N.A. 2013. Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola. Molecular Phylogenetics and Evolution. 68(1), pp.42–54.

Ortiz-Rivas B. and Martinez-Torres D. 2010. Combination of molecular data support the existence of three main lineages in the phylogeny of aphids (Hemiptera: Aphididae) and the basal position of the subfamily Lachninae. Molecular Phylogenetics and Evolution. 55(1), pp.305–317.

Peccoud, J. Simon, J.C. von Dohlen, C. Coeur d’acier, A., Plantegenest, M., Vanlerberghe-Masutti, F. & Jousselin, E. (2010). Evolutionary history of aphid-plant associations and their role in aphid diversification. Comptes rendus biologies. 333(6), pp.474-487.

Recommended: Aphid Ecology, 2nd Edition. A.F.G. Dixon.

Aphid Mysteries – Unraveling the past 

Hi! As you may already know, this year I started my masters in Entomology at Harper Adams University where I’m hoping to nurture my passion for aphids. Luckily, the course has an amazing team of entomologists, including Professor Simon Leather, whose research on aphids I’m a big fan of!

He happened to recommend a paper to me called ‘Aphid Mysteries’ by Heie (2009), a Danish entomologist who has studied aphids extensively. This paper was fascinating, and although it was written relatively recently I was interested to see how much research has since been done on aphids. And so I have decided to write my first blog post about where we are now in aphid research.

Heie’s paper considers questions about aphids which hadn’t been answered by any of the published literature of the time, such. These unknowns are (or were) related to the following:

  • The choice of host plant
  • Host alternation
  • Variation in size of population
  • Morphology
  • Geographical distribution
  • Palaeontology
  • Evolution

This first blog will be split into three sections starting here with the palaeontological evidence of aphids and geographical locations. The other points made above will be addressed in the following two blog posts!

The Origins

The aim of this post is to give a very brief overview of some of the published information on the origins of aphids and their fossils – but by no means will this cover the whole topic in as much detail as the subject may deserve. So think of this as a taster session!

In 2009 (the year of Heie’s journal publication), it was unknown whereabouts in the world aphids originated from – the Northern or the Southern hemisphere? When I delved into the literature on the subject, I found that there was a very mixed consensus, depending on which angle you come from.

Looking at the geographical locations of modern aphids, the majority of species are located in the Northern hemisphere, which is in contrast to most other insects, which increase in biodiversity both at and south of the equator. It would seem safe to assume that this was also the case in their evolutionary history as well. However, some research disputes this assumption. It is thought that the distribution of aphids today is due to a species radiation in some lineages of aphids found in the Northern hemisphere that took place in the Tertiary period. During this radiation, the tropics would have therefore presented a geographical barrier that many species would not have been able to overcome during migration to the South. Another theory about the current distribution of aphids is that they could also be well adapted to colder climates because of the winter host phase in their life cycle (this will be explained further in a future blog – keep your eyes peeled!)

sp-richness-heie-1994

*The species richness of aphids in a number of different areas across the world (from Heie, 1994).

The largest family of aphids, the Aphididae, contains species which are largely present across Northern Asia, Northern Europe and North America. This family is divided into 27 subfamilies, including the Aphidinae which hosts some of the world’s major pest species and dominates temperate regions of the Northern hemisphere and subtropical regions. The wide distribution range of the Aphididae causes some suspicion on the topic of aphid origins. It is thought that the Aphididae likely diverged from a common ancestor, Adelgidae or Phylloxeridae, during the Cretaceous. A study carried out in New Zealand found that endemic aphids of the tribe Aphidini (of the Aphidinae) had been present in the Southern hemisphere from at least the Lower Miocene (23.3 to 15.9 million years ago) and possibly even before then.*The species richness of aphids in a number of different areas across the world (from Heie, 1994).

So what about the fossil records?

It is pretty amazing that aphids have become fossilised considering they have soft bodies and are relatively small in size. But luckily there are quite a few fossil records out there. The fossilised wing of perhaps the most well-known fossil aphid recorded, Triassoaphis cubitus (Evans), was discovered in Australia and would have lived during the Triassic period. Other wing fossils, such as Ceraphis theodora (Shcherbakov) from Middle Asia, and Leaphis prima (Shcherbakov) from the Vosges France, have also been found to date back to the Triassic. The only whole body specimen (or almost –part of the antenna and parts of some of the legs were missing) from the middle Triassic, Dracaphis angustata (Hong), was also discovered in China.

geo-ts

*Geographic Time Scale

There are multiple other fossils specimens that have been discovered from the Cretaceous and Jurassic. Penaphis woollardi (Jarzembowski) was discovered in southern England and is thought to have existed during the Early Cretaceous. It may have been one of the first aphids to feed on the ancient gymnosperms. The first fossil aphid from Africa, Siphonophoroides orapaensis (Rayner) – this species was not confidently assigned to this lineage and has therefore been placed in this genera due to some similarities with other extant species. S. orapaenis was discovered in the Orapa kimberlite crater (amongst many other insects) and is thought to have also existed during the Cretaceous period. A few aphids from Denmark have also been found, such as the alate morph of Diatomyzus eocaenicus (Heie) from the Lower Eocene.

Up until recently, the Triassic was the period which contained the oldest recorded fossil aphids. In 2014 a paper was published on the discovery of an aphid dating back to the Palaeozoic era, in the middle Permian. This new species, Lutevanaphis permiana (Szwedo), found in the Lodève Basin in Southern France, now represents the oldest fossil specimen from the Aphidomorpha currently known.

szwedo-2014-wing

*A) A reconstruction of wing venation pattern. B) Holotype specimen (from Szwedo et al. 2014)

Aphids are also famously closely associated with several other species such as ants, host plants and specialist aphid parasitoids, so is it possible that fossil records of these species could also be used to figure out where aphids originate from?

The ancient gymnosperms that are presumed to have hosted aphids in the past were present in the Southern hemisphere. Although there are few lineages of aphids that are native to the southern hemisphere today, the assumption that they were also there at some point in the past makes sense. (But more on this in the next post!)

geo-plant-ts

*Geographical Time Scale and Plant Evolution

Specialist parasitoids also have close relationships with aphids and are often used as a biocontrol method in controlling aphid population due to their shortened ovipositor that is specially adapted for inserting into an aphid. In 2009 a piece of Albanian amber was recovered from a site in Spain which contained an Aphidiine parasitoid wasp. Research on this species concluded that this ancient and previously undiscovered species, Archephedrus stolamissus (Ortega-Blanco), from the Braconidae, originated from the Northern hemisphere rather than the Southern hemisphere which was previously thought to have been the case. In former literature it was speculated that the Aphidiine originated in the Southern hemisphere based on the location of several Southern genera (see Belshaw in the reference list below). This newer research suggests that members of the Aphidiine were already present in the Northern hemisphere during the later Cretaceous.

ortega-2009-wasp

*Illustration of the Holotype male Archephedrus stolamissus, a new genus and species (from Ortega-Blanco et al. 2009).

The oldest of all described fossil aphids have been discovered either in China or Australia, which may suggest that aphids originally existed in these Eastern parts of the world before spreading into other areas such as Europe. But the evidence of fossil aphids cannot be used alone as there may be some bias in the areas where the most fossils are preserved. When looking at those species that have close relationships with the aphids there is a mixed opinion on their origins and therefore no definite conclusion has been made based on these facts. Based on the fossil evidence it may also be likely that more aphids from earlier time periods just haven’t been discovered yet.

I would love to hear your opinions on this topic so please leave any comments below. The evolution of aphids and their morphology will be continued in the next blog post, which should be up within the next few weeks! Thank you for reading and I hope you find it interesting J See you again soon!

Picture References

Species richness table: from Heie, 1994.

Geographic Time Scale: from https://www.bgs.ac.uk/discoveringGeology/time/timechart/home.html?src=topNav

Geographic Time Scale (plant): from https://www.britannica.com/science/Mesozoic-Era

Holotype specimen & wing venation of Lutevanaphis permiana: from Szwedo et al. 2014.

Holotype male Archephedrus stolamissus: Ortega-Blanco et al. 2009

Text References

Belshaw, R., Dowton, M., Quicke, D.L.J. & Austin, A.D. (2000). Estimating ancestral geographical distributions: a Gondwanan origin for aphid parasitoids? Proceedings of the Royal Society of London B: Biological Sciences. 267(1442), pp.491-496.

Heie, O.E. (1970). Lower Eocene aphids (Insecta) from Denmark. Bulletin of the Geological Society of Denmark. 20(2), pp.162-168.

Heie, O.E. (1994). Why are there so few aphid species in the temperate areas of the southern hemisphere? European Journal of Entomology. 91, pp.127-133.

Hong, Y., Zhang, Z., Guo, X. & Heie, O.E. (2009). A new species representing the oldest aphid (Hemiptera, Aphidomorpha) from the Middle Triassic of China. Journal of Palaeontology. 83(5), pp.826-831.

Jarembowski, E.A. (1989). A fossil aphid (Insecta: Hemiptera) from the Early Cretaceous of southern England. Cretaceous Research, 10, pp.239-248.

Moran, N.A., Kaplan, M.E., Gelsey, M.J., Murphy, T.G. & Scholes, E.A. (1999). Phylogenetics and evolution of the aphid genus Uroleucon based on mitochondrial and nuclear DNA sequences. Systematic Entomology. 24, pp.85-93.

Ortega-Blanco, J., Bennett, D.J., Delclòs, S. & Engel, M.S. (2009). A primitive Aphidiine wasp in Albanian amber from Spain and a Northern hemisphere origin for the subfamily (Hymenoptera: Braconidae: Aphidiinae). Journal of the Kansas Entomological Society. 82(4), pp.273-282.

Peccoud, J. Simon, J.C. von Dohlen, C. Coeur d’acier, A., Plantegenest, M., Vanlerberghe-Masutti, F. & Jousselin, E. (2010). Evolutionary history of aphid-plant associations and their role in aphid diversification. Comptes rendus biologies. 333(6), pp.474-487.

Rayner, R.J. & Waters, S.B. (1989). A new aphid from the Cretacous of Botswana. Paleontology. 32(3), pp.669-673.

Shcherbakov, D.E. & Wegierek, P. (1991). Creaphididae, A new and the oldest fossil family from the Triassic of Middle Asia. Psyche. 98(1), pp.81-85.

Szwedo, J. & Nel, A. (2011). The oldest aphid insect from the Middle Triassic of the Vosges, France. Acta Palaeontologica Polonica. 56(4), pp.757-766.

Szwedo, J., Lapeyrie, J. & Nel, A. (2014). Rooting down the aphid’s tree – the oldest record of the Aphidomorpha lineage from the Palaeozoic (Insecta: Hemiptera). Systematic Entomology. 40(1), pp.207-213.

Von Dohlen, C.D. & Teulon, D.A.J. (2003). Phylogeny and historical biogeography of New Zealand indigenous Aphidini aphids (Hemiptera, Aphididae): An hypothesis. Annals of the Entomological Society of America. 96(2), pp.107-116.

Recommended Authors – Heie & Von Dohlen.

Useful website – http://aphid.speciesfile.org/HomePage/Aphid/HomePage.aspx