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Biology and MorphologyAphid egg production. Egg shape, colour and distribution. Why aphids lay eggs
Aphid egg production
Whilst the great majority of individual aphids are parthenogenetic, nearly every species of aphid can lay fertilized eggs.
The aphid eggs described below are of Aphidoidea, which includes the Aphididae (or 'true aphids'), Adelgidae (sometimes called 'woolly conifer aphids'), and Phylloxeridae. Aphidoidea species undergo cyclical parthenogenesis: Their life-cycle regularly alternates sexual (meiotically-derived) egg-production with one or more generations of asexual (mitotically-derived) egg production.
Whilst Adelgids and Phylloxerids lay eggs produced sexually or parthenogenetically, eggs of true aphids are only laid by females that have mated. As Blackman points out, the parthenogenetic eggs of true aphids are much smaller than fertilized eggs, and develop into first-instar nymphs which are borne live (viviparously).
A female aphid that mates and lay eggs is known as an ovipara (egg-laying morph), rather than the commoner form of aphid female, the vivipara (morph which produces live young). The picture below shows an ovipara (middle-left) of the shiny birch aphid (Symydobius oblongus ) with two eggs (middle-right) she laid by an axial birch bud. The two smaller individuals are probably males.
Some aphids only produce eggs in colder parts of their geographical range. Brachycaudus cardui, for example, has a sexual phase on plum (Prunus) in continental Europe, but not in Britain. Aphid eggs being rather hard to find, when sexual morphs are observed at least some eggs are assumed to result.
A few aphid species such as Myzus ascalonicus, Myzus antirrhinii and Neotoxoptera formosana have not been found to produce sexual forms, and hence have never been known to lay eggs. The same applies to that superabundant pest Myzus ornatus, except possibly in the Himalayas.
Whilst aphid eggs come in a range of sizes, colours and shapes (depending upon the aphid species), eggs are not used to identify aphids. Eggs play little or no part in taxonomic keys, and there is comparatively little egg-related terminology.
Egg shape, colour and distribution
Aphid eggs are variously elliptical to chisel-shaped, and either glued to a support or attached by a thread (as are adelgid eggs, and those of Pineus pini ). The first image (below) shows Adelges cooleyi eggs attached by threads to a needle of Douglas fir, albeit hanging beneath the wax wool produced by their mother. The second image is a micrograph of a Pineus pini egg, showing its attachment thread. This arrangement presumably helps to protect the eggs from predators such as mites.
Newly-laid eggs are relatively light-coloured, and darken as they mature. Below (first) is a freshly-laid Cinara pinea egg on a Pinus sylvestris needle, and (second) two mature eggs (note, no surface wax).
To avoid predators, most (if not all) aphids produce cryptically-coloured eggs. Some species cover their eggs with wax, which may also make them distasteful.
According to Carter & Maslen (1982) Cinara piceicola eggs are "butter yellow when first laid, turning mealy grey colour" - but, under their wax deposit, the new laid eggs are actually honey yellow, and turn black.
ColourIf we ignore the presence or absence of wax, the colour of newly laid eggs is generally cryptic, varying from grey (as in Drepanosiphum platanoidis, below ) through yellow, to dark orange-red (as in Lachnus roboris below ). Below (first) are fresh Symydobius eggs (between axillary bud and stem of birch), and (second) fresh Cinara piceae eggs.
Sclerotized, mature aphid eggs are generally brown or black, to grey, depending upon the degree of wax-coverage. Below (first) are Symydobius oblongus eggs, and (second) a close-up of Chaetosiphon tetrarhodum eggs (on Rosa rugosa).
Some aphids also conceal their eggs under wax 'wool' (produced by the mother). Below (first) are two egg masses of Pineus pini covered by wax wool (on Scots pine), and (second) fresh Adelges cooleyi eggs (held by threads, under the white wax wool produced by their exule).
Spatial distributionThe spatial-arrangement of eggs varies hugely between species.
On evergreen host-plants aphid eggs are commonly laid on leaves. Below (first) are Cinara acutirostris eggs laid single-file along a needle (note the damaged or infertile egg), and (second) Cinara pini (these eggs, being small, are not laid in a single row).
On deciduous hosts eggs are often laid by buds, or on young branches with buds nearby. Below (first) mature Maculolachnus submacula eggs aggregated around a bud on rose (note their ovipara has died in situ following oviposition), and (second) Chaetosiphon tetrarhodum eggs on Rosa rugosa.
Adelges laricis (below ) lays their eggs in clumps where the leaves will emerge.
Many aphids conceal their eggs in crevices near to a ready food supply. Below (first) aggregation of Myzocallis coryli eggs at base of axial bud of recent hazel growth and (second) eggs of Rhopalosiphum padi (laid in autumn in the narrow gap between the axillary buds and the stem).
Leather (1983) estimated there is only enough room in this site for 10-15 eggs to be adequately protected from predators, and has shown that post-oviposition there is a period of density-dependent mortality where eggs in suboptimal sites are predated. Predators include spiders and birds (see below for more on predation of eggs).
Some aphids put their eggs some distance from food. The image (below) shows a mixture of new and mature Drepanosiphum platanoidis eggs in their preferred oviposition site, in bark crevices, low on the tree's trunk remote from a feeding site.
Lachnus roboris oviparae, instead of concealing their eggs, congregate on large branches and lay huge masses of eggs. Presumably the most important predators are 'swamped' by the sheer food abundance (as are lions by huge wildebeest herds). Oviparae of other species, including Maculolachnus submacula, also aggregate when egg-laying.
Lastly a few oviparae, especially old and damaged ones towards the end of the season, lay their eggs in atypical sites - which appear to give these eggs little hope of survival. The first image (below) shows a dying Drepanosiphum platanoidis ovipara producing eggs (they are very pallid when fresh, and have no wax) in an abnormal site. This leaf will soon drop off. The second image (below) shows an old sick Lachnus roboris laying a last lone egg...
Why aphids lay eggs
For aphids, egg-production is primarily a way to survive cold, to a lesser degree to cope with food-scarcity; and least of all to multiply. Those issues aside, nearly all eggs are produced sexually - this link seems ancient, even among eukaryotes.
Cold-avoidanceSome aphid species are remarkably cold-resistant - both aphids & eggs contain antifreeze, but eggs are the most cold resistant. Elatobium abietinum only produces eggs in continental Europe, elsewhere it overwinters in its parthenogenetic form. Egg-production is usually timed to coincide with the onset of cold weather, so most aphid species oviposit in October and November.
Not all aphids wait so late to produce eggs. Eucallipterus tiliae has evolved to cope with sudden drops in the population size of aphids in late summer (caused by predation?) and lays all its eggs before the end of September. Aphis farinosa goes a step further and produces its sexual forms and eggs in mid-summer.
Hunger, aestivation and changing hostApart from the direct effects of low temperatures, there is also the problem of food shortage in winter. Many aphids get through this period by producing a non-feeding stage - the egg. However, cold is not the only cause of food shortage for aphids, and eggs are not the only way to deal with lack of food.
A number of aphid species survive warm(ish) periods of food shortage by dormancy (aestivating) - but about 10% of aphid species move to an alternate host species (usually known as their secondary host or summer host). In most aphid species their summer host is a herbaceous plant species. For some aphid species their only host is a herb species, assumed to be a secondary host - their 'primary host' being unknown, or lost.
If an aphid species host-alternates, the plant host it lays its eggs upon may be described as its primary host, or (aside from the adelgids) the winter host (adelgids' host-alternation is not seasonal but annual.) For most aphid species their primary host is a woody plant species - but, if the only host is a herb, some species lay eggs on that 'secondary host'. For instance Macrosiphoniella tanacetaria and Metopeurum fuscoviride lay eggs on Tansy. Hyalopteroides humilis, whilst mostly parthenogenetic in UK, lays eggs on cocks-foot grass in Europe.
Multiplication & survivalWhilst a single ovipara (sexual, egg-laying form) can produce quite a few eggs, few survive to hatch - or reproduce. The vast majority of aphid nymphs are born, live, by parthenogenetic viviparae.
Eggs being immobile, many are lost to predation. The first image (below) shows a mature but damaged Myzocallis coryli egg, (left) and the presumed culprits (right). The second image is a close-up of a mite feeding on the egg.
Damaged eggs can be very common, Kulman (1967) found 70-90% of eggs of woolly pine needle aphid (Schizolachnus piniradiatae) did not hatch. In contrast Way & Banks (1964) thought that average mortality of Aphis fabae eggs was unlikely to exceed 40%, and was probably relatively unimportant in limiting the subsequent increase in numbers.
Some eggs are predated or killed by pathogenic fungi, some are not fertilized and others are damaged by their own mothers.
Whilst there are reports of adult behaviour consistent with caring for nymphs (e.g. Uroleucon tanaceti ), we know of no examples of aphids caring for eggs after laying them. This is understandable since a viviparous female is twice as closely related to her parthenogenetically-produced nymph as an oviparous female is to her fertilized egg. The first image (below) shows a Lachnus roboris ovipara astride a newly-laid egg-mass (not all of which are hers!). Note what her middle foot is doing to one egg. The second image shows a number of damaged eggs exuding drops of orange fluid. Presumably tending ants similarly damage freshly-laid eggs.
That said, ants protect and groom unhatched eggs of some aphid species, presumably in the expectation of honeydew to come. Matsuura & Yashiro (2006) observed that without ants, aphid eggs were rapidly killed by fungi. Grooming by the ants protected Stomaphis hirukawai eggs, at least, against pathogenic fungi. We have observed similar grooming by ants attending eggs of Adelges laricis and Lachnus roboris. The first image (below) shows a Southern Wood ant (Formica rufa) guarding fresh and mature Adelges laricis eggs. Note the dead sistens. The second image is a mature egg-mass of Lachnus roboris. Ants tend oviparae when around, and groom the eggs in spring after females have died.
The survival of nymphs hatched from eggs depends upon food being available (whether sap rise, bud swelling, leaf or shoot growth) shortly after their emergence - for aestivating individuals this is rather less crucial.
RecombinationAmong the Aphididae (=true aphids), meiotic recombination has only been observed in ovipera, and eggs are only produced by oviparae after mating with males. However it seems likely that ancestral Aphidoidea reproduced by cyclical parthenogenesis, and most eggs were produced asexually.
Unlike humans, which bear live young and seldom reproduce asexually, adelgids can produce eggs parthenogenetically, and some adelgid species do so exclusively. Species such as Adelges cooleyi, which produce eggs sexually, do so on their primary host - Larch. Adelges abietis eggs commonly remain within the body of their (parthenogenetic, gallicola) mother post-mortem - perhaps this helps protect the eggs from mites? Notice eggs from a ruptured body remain attached by threads.
Assuming aphids evolved in temperate latitudes, the link between recombination and egg-production on a primary host is a historical legacy. Nevertheless some aphids engage in recombination extremely rarely, as do bacteria. A number of aphids are anholocyclic - they reproduce parthenogenetically all year round without a sexual phase. In other words, their sexual forms have never been observed. This does not imply sexual forms never occur - they may be extremely rare, or only occur in a restricted locale. Nor does it imply clones within an aphid species are genetically identical (sexual reproduction does not introduce genetic variation, it merely redistributes it).
We may conclude that, although most species retain sexual reproduction, recombination is not a priority for aphids.