It is generally accepted that ancestors of Sternorrhyncha (the aphids, adelgids & phylloxerids) were like other Hemiptera: They reproduced via eggs (Ogawa & Miura, 2014 ) following sexual reproduction (Hales et al. 1997 ). However, whilst it is tempting to assume all adults were winged, many hemiptera exhibit brachypterous / macropterous forms. (e.g. see here ).
Whilst remaining egg-laying, the Sternorrhyncha evolved to alternate sexual reproduction with one or more generations of asexual reproduction (=cyclical parthenogenesis).
- From the Greek, polumorphos:
polu (=many) + morphe (=form)
- The coexistence, in the same locality, of two or more distinct forms independent of sex, not connected by intermediate gradations, but produced from common parents.
Modern aphids (=Aphididae) probably began as temperate tree-dwelling species, then diversified along with flowering plants (Von Dohlen, 2000 ). Yet, as Blackman found, half their species still live on trees for at least part of their lifecycle (as do the other modern Sternorrhyncha: Phylloxeridae and Adelgidae). Unlike other Sternorrhyncha, aphids only lay eggs following sexual reproduction (usually in autumn), and are viviparously parthenogenetic for the rest of the time. Aphids now have far more species than Phylloxerids and Adelgids, and some aphid species have many body forms - others very few.
Consider these four examples:
- Neomyzus circumflexus has never been found to have sexual forms (its primary host is 'lost'), but reproduces parthenogenetically via viviparous females (=viviparae). Their nymphs mature into just two adult forms, winged or wingless - either of which can produce winged or wingless offspring.
- Drepanosiphum platanoidis is a single-host species, which reproduces by cyclical parthenogenesis. For most of the year all the adults are green winged-viviparae - but in late spring nymphs mature into very pale, winged, viviparae that diapause during summer, then produce normal winged viviparae. In autumn, viviparae produce nymphs that mature to sexual forms: either winged sexual males, or wingless egg-laying sexual females - known as oviparae.
The 2 seasonal-forms (normal, & aestivating adult) and 2 sexual-forms (male, & ovipara) are shown below.
- Rhopalosiphum padi alternates host seasonally. On their primary-host nymphs, hatched from sexually-produced eggs, mature to distinctive wingless fundatrices (=founding-mothers, one shown with nymphs below). Their daughters and granddaughters are also wingless, but covered with gray mealy wax (see below), and produce leaf-roll galls. Crowding and poor nutrition eventually causes their gall-dwelling offspring to mature into greenish winged forms (below) which fly to their secondary host. Viviparae maturing on the secondary host are wingless (below), or winged, and are greenish with a rust-red suffusion around the base of each siphunculus. In autumn winged forms (known as gynoparae, not shown) return to the primary host, where their nymphs mature to wingless (oviparae). Later in autumn viviparae on the secondary host switch to producing winged males, which fly to the primary host to mate with the oviparae (both shown below).
Below are: a fundatrix with her wax-covered nymphs, wax-covered adults & nymphs in their gall, a winged emigrant on the primary host, a colony on their secondary host, and a winged male with oviparae on the primary host.
- Paracletus cimiciformis host-alternates, with a minimum 2-year cycle. (Salazar, et al., 2015 ) On their primary host, nymphs, hatched from eggs, mature to distinctive gall-forming wingless fundatrices. These fundatrices produce leaf-galls, and their nymphs become wingless viviparae specialized for gall-dwelling. These viviparae reproduce themselves in the galls until autumn, then produce winged forms. These winged adults fly to their secondary host, where their nymphs mature to round green, wingless, root-feeding, ant-attended viviparae. Their nymphs either mature to round green wingless viviparae, or to flat white viviparae which feed on the haemolymph of ant larvae. Their nymphs mature to flat white forms or, in autumn, to two different winged forms: One winged form gives rise to round green wingless root-feeding ant-attended viviparae. The other winged form flies to the primary host, and produces wingless sexual-forms (males and oviparae).
Some aphids, particularly host-alternating species, are unusual in having many distinct forms like social insects (bees, wasps, ants, & termites have 'casts'). A few gall-forming aphids are considered social, and have up to a dozen forms, including defensive (soldier) forms.
The multitude of possible aphid body forms has some important consequences:
- They enable aphids to optimize for growth, reproduction, dispersal, aestivation, symbiosis, host-adaption and defence. - And to be optimized for one or more of those roles. Given which, the forms produced for any one species may vary seasonally.
- Multiple body forms make life hard when trying to identify an aphid - especially for seasonal or seldom observed forms.
- Owing to their rather unusual biology, the terminology for aphid forms is (frankly) rather a mess.
Morphs, polymorphs and phenomorphs
Originally 'morph' just applied to visible traits (such as winged/wingless, or red/green), but this is no longer so.
- For example, some aphid species produce two outwardly-indistinguishable winged viviparous forms: one form can fly, the other cannot.
- Conversely, winged aphids, upon reaching a new host, tend to optimize their reproductive capacity by autolysing their wing muscles. Whilst impairing their flying ability, it does not change their morph.
- A morph is the name given to specific groups of insects that are all of the same species but differ in appearance.
Unfortunately, 'morph', which you might assume to be equivalent to 'body form' - as in 'morphology' - has acquired so many usages and definitions as to be almost meaningless - and this confusion extends to its use as a suffix.
One source of difficulty is that, whilst a few aphid body forms are dictated genetically (=genomorphs), most forms are dictated environmentally but not genetically (=phenomorphs).
- A phene is an individual genetically determined characteristic or trait which can be possessed by an organism, such as eye colour, height, behaviour, tooth shape or any other observable characteristic. ... Phenotype refers to a collection of Phenes possessed by a particular organism.
- All of the body forms we listed above, including males, but excluding fundatrices, are produced by parthenogenetic viviparous reproduction.
- Aside from the occasional very rare mutation, every parthenogenetically-produced female is genetically identical to her sisters, daughters and mother - which are therefore clones.
- Every female form with a clone, including the oviparae and fundatrix, is therefore produced from an identical genetic blueprint (=genotype). Each body form evidently results, not from different genes, but from different sets of genes being switched on.
- The only genetic difference between a male aphid and his mother is she has two sex chromosomes, he has one, and brothers may vary accordingly.
- Thus Acyrthosiphon pisum males can be wingless or winged depending upon which sex chromosome they happen to inherit (Braendle et al., 2006 ). Some clones produce only winged males, some yield only wingless males, and some give both.
Given so many body forms can be achieved by switching genes on or off, changing from one form to another sounds deceptively simple. Indeed it is commonly but wrongly assumed that 'morph', in zoology, is shortened from 'metamorphosis' - and implies plastic changes of form or appearance. However, unlike chameleons, once an aphid has matured into a particular form, it cannot change to another. Also, since intermediate forms tend to be sub-optimal, form-selection is generally an all-or-nothing choice. Intermediate forms are rare.
- For example, whether viviparae are winged or wingless is often determined by conditions such as crowding or nutrition whilst an aphids is an embryo, or an early nymph. Occasionally those conditions change suddenly, causing adults to have intermediate form - such as the brachypterous (=reduced wings) Symydobius oblongus.
Below are: a normal winged form; and a (rare) brachypterous form next to a normal wingless form.
'Morph' does not refer to atypical forms, local variants, malformed-individuals, nor to a continuous variable such as body-length, unless it has a strongly bi-modal or polymodal distribution (individual size commonly varies due to diet or maturity).
Given the number of body forms potentially available within an aphid clone, much work has been invested in understanding what determines a particular body form, and how flexible that choice is.
- Some body forms, it appears, must appear in a pre-determined sequence. For example, a fundatrix form (if such exists) must come first, then viviparous forms, and sexual forms last.
- One exception is Acyrthosiphon svalbardicum, which lives at very high latitudes, and commonly omits viviparous forms (Hales et al., 1997 )
- Trying to accelerate the transitions from fundatrix to autumn-migrants, or sexual forms, by for instance temperature changes, indicates aphids have a built-in 'interval timer' to prevent this (a minimum number of days, not generations, must elapse).
- Many attempts have been made to produce adults normal to the primary host by moving viviparae from the secondary host ahead of the time when such flights usually occur (or to the secondary from primary). Such aphids generally feed poorly and die, but their progeny do not change morph. Indeed, it has been suggested that a crucial factor limiting the evolution of host-alternating aphids is their fundatrices are highly specialized to, hence dependent upon, their primary host (Moran, 1988 ).
- Many aphid species produce both winged and wingless viviparae. In some species either of these forms can give rise to either of the other. The stimulus to produce winged viviparae is often crowding, but in host-alternating species night-length and temperature can be more important.
- Some species produce viviparae in several distinct, alternative, colour-forms. These forms tend to produce offspring of the same colour, and in some species these forms may also be winged or wingless. Whilst distinct colour-forms commonly arise within clones (presumably by switching on sets of genes) they can also be caused by bacteria, or by genetic differences.
Acyrthosiphon pisum green and red forms (shown below) appear to be maintained by balanced selection from a predator (Coccinella septempunctata) and a parasitoid (Aphidius ervi). When parasitism rates were higher than predation rates, red morphs were at an advantage.
A number of biologists feel these latter two (#4&5), alternate phenotypic, sets of forms be known as 'phenomorphs' or 'morphs' - but genetically determined alternatives (such as winged and wingless males) be termed 'genetic polymorphs'.
Distinctive morphs are not limited to adult forms.
A number of aphid species produce forms optimized, to some degree, for defense.
- Adults of Chaitophorus or Pterocomma species bear a large and specialized cauda, which holds their honeydew ready for ant-collection. The ants, in turn, discourage birds - and even browsing herbivores. Since all adults of those species are thus equipped, this is a monomorphic character.
- As Simon Leather describes, first instar nymphs of the gall-forming species Pemphigus betae fight each other for possession of an optimal galling site, whereas Epipemphigus niisimae fight for the gall.
- A number of Pemphiginae aphids and Hormaphidinae aphids (tribes Pemphigini, Eriosomatini, Fordini; and Hormaphidini, Cerataphidini, Nipponaphidini), having formed a gall, produce nymphs optimized to defend it - &/or to repair damage (Pike & Foster, 2008 ). These are commonly first-instar nymphs, but some use later instars. What proportion of nymphs are soldiers varies between species, but we found Hamamelistes betulinus appears, monomorphically, to produce partially-sclerotized first-instar nymphs with strengthened legs (shown below).
- Braendle, C., Davis, G.K., Brisson, J.A. & Stern, D.L. (2006). Wing dimorphism in aphids. Heredity 97, 192-199. Full text
- Hales, D.F, Tomiuk, J., Wöhrmann, K. & Sunnucks, P. (1997). Evolutionary and genetic aspects of aphid biology: A review. European Journal of Entomology 94, 1-55. Full text
- Inbar, M. (1998). Competition, territoriality and maternal defense in a gall-forming aphid. Ethology Ecology & Evolution 10, 159-170. Full text
- Moran, N.A. (1988). The evolution of host-plant alternation in aphids: evidence for specialization as a dead end. The American Naturalist 132(5), 681-706. Abstract
- Ogawa, K. & Miura, T. (2014). Aphid polyphenisms: trans-generational developmental regulation through viviparity. Frontiers in Physiology 5, 1-11 doi: 10.3389/fphys.2014.00001 Full text
- Pike, N. & Foster, W.A. (2008). The ecology of altruism in a clonal insect. In: Korb, J. & Heinze, J. (eds). Ecology of social evolution. Springer. 266pp. Full text
- Salazar, A., Fürstenau, B., Quero, C., Pérez-Hidalgo, N., Carazo, P., Font, E. & Martínez-Torres, D. (2015). Aggressive mimicry coexists with mutualism in an aphid. PNAS 112(4), 1101-1106. Full text
- Von Dohlen, C. (2000). Molecular data support a rapid radiation of aphids in the Cretaceous and multiple origins of host alternation. Biological Journal of the Linnean Society 71, 689-717. doi:10.1006/bijl.2000.0470 Full text