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Evolutionary Ecology

, Volume 33, Issue 1, pp 1–19 | Cite as

Evolutionary ecology of insect egg coloration: a review

  • Eric Guerra-GrenierEmail author
Article

Abstract

Body coloration in animals is often adaptive and used for defense against biotic (e.g., predators, competitors) and abiotic (e.g., solar radiation, desiccation) threats. The study of adaptive coloration in insects usually favors obvious model species such as yellowjacket wasps (Vespula spp.) and longwing butterflies (Heliconius spp.), partly because they actively interact with their environment. Yet, one life stage has received less attention because of its immobility: the egg. So far, vertebrate eggs, especially avian eggs, have held the ‘‘big end of the stick’’ when it comes to research effort on adaptive egg coloration. In species where eggs are not provided with parental care and left to survive on their own until hatching, studying the defensive roles played by their colors is imperative to understand their evolutionary ecology. Adaptive functions provided by egg coloration such as crypsis, aposematism and photoprotection against ultraviolet radiation potentially have huge fitness impacts and deserve more attention. Here, the current literature on insect egg coloration is reviewed, reporting its known adaptive significance. Clear distinctions are made between functions tested empirically and functions that remain hypothetical despite often being treated as facts. Avenues for future work in the field are also provided.

Keywords

Defense mechanisms Adaptive coloration Crypsis Warning signals Masquerade Ultraviolet radiation 

Introduction

Since the publication of The Colors of Animals (Poulton 1890), evolutionary biologists have studied and significantly improved our understanding of animal coloration and its functions in nature (Cuthill et al. 2017). We now know that colors are used by a plethora of taxa in various ways. In many species, body coloration is sexually selected to communicate mate quality between sexes, usually from the male to the female (Endler 1983; Hill 1991; Maan and Cummings 2009). Colors are also frequently integrated in defensive strategies against predators, either to conceal the prey (e.g., background-matching camouflage) or to advertise its unprofitability, whether the signal is honest (e.g., aposematism, Müllerian mimicry) or not (e.g., Batesian mimicry) (Ruxton et al. 2004). Furthermore, coloration can allow animals to interact with their abiotic environment and confer fitness benefits through thermoregulation (Forsman 2000), photoprotection against ultraviolet radiation (Jablonski and Chaplin 2000) and water retention (Välimäki et al. 2015).

When we think of adaptive coloration, especially in the context of predator–prey relationships, we tend to picture free-living, mobile organisms such as adult peacocks, chameleons, skunks and bees. Yet, eggs are also often very colorful. It can be argued that color-related defenses in eggs are potentially more important than in mobile life stages, as the former are fixed in space until hatching and cannot flee like the latter if discovered by predators. A considerable amount of work has been done on chordate egg coloration in taxa such as ascidians (Young and Bingham 1987) and amphibians (Petranka et al. 1998; Altig and McDiarmid 2007; Pintar and Resetarits 2017), but especially in birds. Kilner (2006) reviewed the adaptive significance of bird egg coloration and listed multiple functions such as camouflage and thermoregulation. Blues in egg shells are of particular interest, as they are used for their photoprotective properties (Bakken et al. 1978) or to signal maternal investment in egg nutrients as a way to elicit parental care from sires (Moreno and Osorno 2003; Soler et al. 2005). The interest for blue shell coloration even led to recent discoveries on its presence in dinosaur lineages (Wiemann et al. 2017). Egg color is also used for mimicry in brood parasites such as cuckoos, as a way to reduce the host’s ability to discriminate between the parasite’s eggs and its own (de Brooke and Davies 1988; Stoddard and Stevens 2011).

Compared to vertebrates, we know a lot less about the adaptive significance of invertebrate egg coloration. Yet, the latter group largely outnumbers the former in terms of biodiversity, with an estimated 7 million species worldwide just for terrestrial arthropods (Stork 2018). Among what can only be described as a small fraction of the species diversity in which egg coloration has been studied, a few examples of aposematic eggs have been reported in aquatic invertebrates. For example, the pink-red egg ribbons of the Spanish dancer nudibranch, Hexabranchus sanguineus (Ruppell and Leuckhart 1828), contain toxic macrolides sequestered from their sponge-rich diet (Pawlik et al. 1988). Apple snails of the genus Pomacea also produce pink eggs using carotenoids, which are defended thanks to a proteinase inhibitor called ovorubin (Dreon et al. 2010). As far as insect eggs go, not much is known about the fitness benefits of their coloration, regardless of how morphologically diverse they are.

The aim of this paper is to review the current state of knowledge regarding the adaptive significance of insect egg coloration. Reviews on insect egg defenses (Hinton 1981; Blum and Hilker 2002) and parental investment (Wong et al. 2013) have been published in the past, but there remains a significant gap in the literature that needs to be filled regarding color-related defensive strategies. Although the work that has been done on non-adaptive physiological color change during development (Peterson 1962; Bernhardt 2009) and on the use of colors by egg parasitoids as a foraging cue (Lobdell et al. 2005) is acknowledged, the focus of this review will be solely on adaptive egg coloration. This paper is therefore divided into multiple categories, each one reviewing a given adaptive function such as crypsis, warning signals and photoprotection. Where necessary, distinctions are made between conclusions based on experimentation versus on educated guesses.

Methodology

Papers were collected for review using Google Scholar and Web of Science. Key words used to search for studies included (1) insect egg coloration; (2) insect egg colouration; (3) insect egg camouflage; (4) insect egg crypsis; (5) insect egg mimicry; (6) insect egg masquerade; (7) insect egg aposematism. Papers were included in the review as long as they provided a hypothesis for the adaptive significance of egg coloration of at least one insect species (with the exception of papers listed in Table 1, which were included as long as they looked at insect egg chemical defenses). Papers cited by or citing the studies found using search engines and fitting the inclusion criteria were also included in the review. Overall, the studies here reviewed were published between 1962 and 2017. Collection of papers was concluded in September 2018.
Table 1

Non-exhaustive list of insect species with known egg chemical defenses

Order

Family

Species

Defensive compound(s)

Egg color reported?

Aposematism hypothesized?

Indirect evidence of aposematism?

Direct evidence of aposematism?

References

Coleoptera

Chrysomelidae

Acalymma vittatum

Cucurbitacins

No

No

Ferguson et al. (1985)

Chrysolina coerulans

Cardenolides

No

No

Daloze and Pasteels (1979)

Chrysolina fuliginosa

Cardenolides

No

No

Hilker et al. (1992)

Chrysolina polita

Cardenolides

No

No

Daloze and Pasteels (1979)

Chrysomela spp.

Isoxazolinone glucosides and salicin

Brightly colored

No

Pasteels et al. (1986)

Dibrotica spp.

Cucurbitacins

No

No

Ferguson et al. (1985)

Galeruca tanaceti

Anthraquinones

No

No

Hilker and Schulz (1991)

Gastrophysa cyanea

Oleic acid

Yellow

Yes

Howard et al. (1982a)

Oreina elongata

Cardenolides and pyrrolizidine alkaloids

No

No

Pasteels et al. (1996)

Paropsis atomaria

Cyanogenic glycosides

No

No

Nahrstedt and Davis (1986)

Phratora spp.

Isoxazolinone glucosides and salicin

Brightly colored

No

Pasteels et al. (1986)

Plagiodera versicolora

Isoxazolinone glucosides and salicin

Brightly colored

No

Pasteels et al. (1986)

Pyrrhalta luteola

Anthraquinones and Anthrones

No

No

Howard et al. (1982b)

Coccinellidae

Adalia bipunctata

Alkaloids

No

No

Lognay et al. (1996)

Adalia decempunctata

Alkaloids

No

No

Lognay et al. (1996)

Coccinella septempuncta

Alkaloids

Yellow/orange

Yes

Positive correlations between egg color metrics and toxicity

Winters et al. (2014)

Exochomus quadripustulatus

Alkaloids

No

No

Daloze et al. (1994)

Exochomus varivestis

Alkaloids

No

No

Daloze et al. (1994)

Lampyridae

Ellychnia corrusca

Lucibufagins

No

Mentioned for free living stages only

Smedley et al. (2017)

Photuris spp.

Betaine and Lucibufagins

No

No

González et al. (1999)

Hemiptera

Dactylopiidae

Dactylopius confusus

Anthraquinines (carminic acid)

No, but hinted that they are red

Mentioned for free living stages only

Eisner et al. (1980)

Lygaeidae

Caenocoris nerii

Cardenolides

Buttercup-yellow

Yes

Von Euw et al. (1971)

Oncopeltus fasciatus

Cardenolides

No

Mentioned for free living stages only

Duffey and Scudder (1974)

Lepidoptera

Erebidae

Cosmosoma myrodora

Pyrrolizidine alkaloids

No

Mentioned for free living stages only

Conner et al. (2000)

Creatonotos transiens

Pyrrolizidine alkaloids

No

No

von Nickisch-Rosenegk et al. (1990)

Utetheisa ornatrix

Pyrrolizidine alkaloids

No

No

Dussourd et al. (1988) and Eisner et al. (2000)

Lycaenidae

Eumaeus atala florida

Cycasin

Whitish/beige with a bright orange/red scale cover

Yes

Rothschild (1992)

Nymphalidae

Actinote spp.

Cyanogenic components

Brightly colored

Mentioned that eggs are colorful and rarely preyed upon

Brown and Francini (1990)

Danaus gilippus

Pyrrolizidine alkaloids

No

Mentioned for free living stages only

Dussourd et al. (1989)

Danaus plexippus

Cardenolides

No

Mentioned for free living stages only

von Reichstein et al. (1968)

Papilionidae

Atrophaneura alcinous

Aristolochic acids

Reddish orange

Yes

Nishida and Fukami (1989)

Parnassius phoebus

Sarmentosin (cyanoglucoside)

No

Mentioned for free living stages only

Nishida and Rothschild (1995)

Various

Various

Various

Various

Yes

Marsh and Rothschild (1974)

Orthoptera

Pyrgomorphidae

Poekilocerus bufonius

Cardenolides

No

Mentioned for free living stages only

von Euw et al. (1967)

Poekilocerus pictus

Cardenolides

No

Mentioned for free living stages only

Pugalenthi and Livingstone (1995)

For each species listed, mentions of egg coloration and aposematism in the original research papers are reported when existent. The symbol “–” is used when studies lacked experimental evidence testing for the aposematism hypothesis

Crypsis

Hiding their eggs is a very efficient way for parents to protect their offspring against natural enemies. A common strategy is to physically hide the offspring, using scales or setae (in Lepidoptera; Hinton 1981), or even sticky spumaline that accumulates dust particles (Peterson 1962). The present section of this review will however focus on ways to hide eggs in plain sight, using only coloration.

Background-matching camouflage

First of all, crypsis does not always have to be achieved through applying colors on the eggs. Background matching can indeed occur simply through transparency. If eggs or egg clutches are transparent, their perceived coloration will be that of the underlying substrate (e.g., a leaf, a twig, bark, etc.) as reflected light from the background around the eggs will presumably be the same as the reflected light coming through the eggs. Several moth species of the Pyralidae and Olethreutidae families have been reported to have transparent shells that make them look like they have the same color as the background (Peterson 1962). Whether this provides a fitness benefit, by making the eggs hard to find by predators, remains untested.

Many insect eggs on plant leaves do however have an intrinsic green or yellowish-green coloration. The most probable explanation for these phenotypes is that green eggs match the color of the substrate they were oviposited on, reducing the risk of being found by natural enemies foraging using visual cues, again through background-matching camouflage. Although this hypothesis is straightforward, it has seldom been tested. For example, the hawkmoth Manduca sexta (L., 1763) is known for its green coloration in eggs (Fig. 1) and caterpillars (Kawooya et al. 1985; Kang et al. 1995). Biochemical assays revealed that the green color is achieved through a mix of yellow carotenoids and insecticyanin, a blue biliprotein sequestered from the hemolymph (Kang et al. 1995). Although this coloration pathway has been hypothesized to create a cryptic effect through background matching, research effort never reached the testing phase.
Fig. 1

Eggs of Manduca sexta laid on a green leaf. The greenish color of the eggs may have evolved for background matching crypsis. Photo by the Insect Zoo of the Smithsonian National Museum of Natural History (CC BY-NC 2.0)

Yellow-green polymorphisms in eggs laid on more than one type of substrate would also make sense in a background-matching camouflage paradigm. Such polymorphism has thus far been identified in at least two species of Lepidoptera: Agathymus estelleae (Stallings and Turner 1958) (Stallings and Stallings 1986) and Papilio aristodemus Esper, 1794 (Daniels et al. 1993). In the former case, females lay eggs that are either green or beige. Glueless eggs are dropped on host plants and some of them fall on the ground while others get lodged on the plants. Stallings and Stallings (1986) reported that green eggs appeared cryptic on the plant while beige eggs were cryptic on the ground, and suggested that egg color dimorphism was used in order to always have a proportion of eggs camouflaged, regardless of where they fall. As for the latter case, Daniels et al. (1993) reported that P. aristodemus can lay either yellow or green eggs on either yellowish or greenish leaves, also as a way to ensure that at least some of the eggs are protected through background-matching camouflage.

Neither study mentioned above, however, actually tested whether the observed egg colorations were cryptic or not. The validity of their hypotheses is not questioned herein, but it is important to stress the problem of confusing hypothesis and fact. Although both papers are interesting and provide promising observations, none of them can conclusively ascertain that egg color in those species is used for background-matching camouflage. Their explanations for the evolution of dimorphic egg coloration are hypothetical and do not consider alternative hypotheses such as the exploitation of search images by predators to reduce the efficacy of predator foraging (Bond 2007). Furthermore, as is the case for other adaptive functions of coloration, camouflage is not selected for by humans, but rather by ecologically relevant predators (Bennett et al. 1994). Quantifying camouflage according to predator color vision and acuity is necessary in order to fully test whether a prey is cryptic or not.

Disruptive camouflage

Contrarily to background-matching camouflage, disruptive camouflage allows prey to go unrecognized, not because they blend with the substrate they are on, but rather thanks to conspicuous markings that either disrupt body edges or create false boundaries, making it difficult to detect as suitable prey (Stevens and Merilaita 2009). Such markings, usually in the form of spots or stripes, are not uncommon in insect eggs. Hinton (1981) argued that the very bold markings on the eggs of the lappet moths Gastropacha quercifolia (L., 1758) and Epicnaptera americana (Harr., 1841) are excellent examples of cryptic eggs that have a disruptive color pattern. Although this hypothesis is likely, it was reported as being the “clear” explanation without ever being tested empirically. Thus, although disruptive coloration in eggs is likely to have evolved in many taxa, concrete evidence of its existence appears to still be missing.

Warning signals

Inter-specific (aposematic) signals

Poulton (1890) originally defined the term aposematism as the use of colors to “warn an enemy off”, usually about antipredation strategies like toxicity (Skelhorn et al. 2016). Such is the case with the yellow-and-black body coloration of venomous wasps or the orange-and-black colors of poisonous Monarch butterflies. Yet, description of aposematic colors in egg entomology is not always adequate. For example, Hinton (1981) used the term to refer to conspicuous colors in general, regardless of their functions. He wrote about color changes from cryptic to aposematic when the process in question was simply caused by the formation of the not yet sclerotized embryo and had nothing to do with the advertisement of secondary defenses.

Orians and Janzen (1974) stated that “insect eggs are almost invariably white or cryptically colored”, yet it is well known among entomologists and naturalists that brightly colored eggs are far from anecdotal in several orders. Multiple studies, reviewed by Blum and Hilker (2002) or published afterwards, have looked at insect egg chemical defense, but only a handful of them reported egg coloration (28.6%), fewer hypothesized aposematism (17.1%) and only one (Winters et al. 2014) tested for it (Table 1). Based on what has been reported on insect egg chemical defenses, we can state that there is a missing link between color and toxicity or unpalatability in the literature. This knowledge gap could be explained by the fact that, so far, egg chemical defense has mostly been of interest to chemical ecologists rather than to evolutionary biologists.

Much like with studies on background-matching camouflage, colorful and toxic eggs are sometimes reported as being aposematic even without empirical data in favor of the hypothesis. For example, Rothschild (1992) stated that the bright yellow eggs of three given insect species “must be deemed aposematic” since they are both conspicuous and toxic. Although this statement was appropriate in the sense that it did not contradict Poulton’s definition of aposematism, it can be argued that the warning function of conspicuous colors should be tested experimentally and not simply assumed. Certain colors that appear conspicuous against their background to humans may not be conspicuous to their predators and parasitoids. Indirect evidence of aposematism can include, for example, correlational data between color and defensive compounds, such as those found between color metrics and alkaloid concentrations in the ladybug Coccinella septempunctata (L., 1758) (see Fig. 2 for a picture of the eggs in question) (Winters et al. 2014). Direct evidence of aposematism, however, requires data on associative learning between color and toxicity by predators. No study to date seems to have provided this kind of evidence. Associative learning by insect predators should not be underestimated, as insects have been shown to learn on several occasions (Dukas 2008) and could therefore realistically associate colors and toxicity or unpalatability.
Fig. 2

Egg clutch of the ladybug Coccinella septempunctata. The orange eggs contrast with the green background, and their color hue and saturation positively correlate with their concentration in defensive alkaloids (Winters et al. 2014). Photo by Gilles San Martin (CC BY-SA 2.0)

Assuming that aposematic displays are the only possible explanation for the presence of both conspicuous egg colors and defensive compounds is also a trap that should be avoided. An alternative hypothesis for their simultaneous presence is the idea that eggs with transparent shells contain pigments, usually carotenoids that cannot be synthesized by the insect, to be used by free-living life stages for warning signals before dietary sequestration of further pigments is available. In such a scenario where predators do not learn to associate color and unprofitability, laying eggs in clutches can instead allow for the protection of some of the offspring (Stamp 1980). Sampling only a fraction of a toxic clutch would be sufficient to deter predation on the rest of it; no need for learning as predation reduction is instead achieved through safety in numbers. Evidence in favor of this hypothesis has been provided by a study describing the foraging behavior of a lacewing larva attacking the eggs of Utetheisa ornatrix (L., 1758) (Lepidoptera, Arctiidae) (Eisner et al. 2000). The authors showed that the proportion of eggs within a clutch eaten by the predators was significantly higher in alkaloid free clutches than in alkaloid-laden clutches.

Intra-specific warning signals and egg load assessment

Warning signals do not necessarily target other species such as predators or inter-specific competitors; they can also be directed towards conspecifics (Sherratt and Forbes 2001). In insects, coloration can be used to allow gravid females to assess the degree of colonization of an individual host plant by conspecifics. Such is the case in the pipevine swallowtail butterfly Battus philenor (L., 1771), in which the conspicuous coloration of the caterpillars, in addition to being an aposematic signal, deters adult females from ovipositing on the same host (Papaj and Newsom 2005). This is thought to reduce intraspecific competition. As for insect eggs, Shapiro (1981a) reported a similar function for the orange-red egg coloration of some species of Pierinae and Euchloinae (Lepidoptera: Pieridae). He carried out a field experiment in which he removed freshly laid eggs from host leaves, four to five times per day. The results showed that “cleaned” plants were used for oviposition significantly more frequently than control plants in which eggs were never removed. In other words, gravid females use the presence of conspecific eggs as a cue to determine whether a host plant is suitable or not. The experiment did not control for egg color and could thus not tease apart the effect the red color from the effects of egg shape or smell. However, Shapiro (1981a) also reported that only species that lay red eggs, as opposed to those with yellowish-white eggs, engage in egg-load assessment, which would suggest (but not confirm) that the red coloration of the eggs functions as an intra-specific warning signal advertising a risk of competition.

Egg-load assessment using egg morphological traits, coloration or otherwise, has sometimes selected for the parasitism of intra-specific warning signals by other organisms. Indeed, some plants have evolved egg mimicry to reduce the risk of oviposition by their herbivores. Such a trait has been described in Passiflora spp. attacked by Heliconius butterflies (Gilbert 1975) as well as in Streptanthus spp. attacked by Pierines (Shapiro 1981a). In all reported cases, leaves develop callosities with shapes and sizes consistent with the morphological features of the eggs laid by their associated herbivores. In the PassifloraHeliconius system specifically, Gilbert (1975) reported that the egg mimics found on the leaves are closer in coloration to old Heliconius eggs than they are to fresh eggs. He argued that this deterred females from laying on the leaves since the caterpillars are cannibalistic and therefore the fake “old” eggs would hatch before and prey upon the real eggs. The adaptive significance of egg mimicry by plants has been confirmed experimentally: artificial removal of egg mimics lead to an increase in oviposition by female butterflies (Shapiro 1981b; Williams and Gilbert 1981). In other words, females maladaptively use the presence of egg mimics to assess the suitability of a host plant. Termite egg recognition can similarly be exploited by other species; inquiline mites (Haifig and Costa-Leonardo 2008) and fungi (Matsuura et al. 2000; Matsuura 2006) have been reported to mimic termite egg color and morphology as a way to benefit from the host nest while avoiding detection and eviction.

Mimicry

Mimicking leftover shells post-parasitism

The most common forms of protective mimicry encountered in nature are Batesian (Bates 1862) and Müllerian mimicry (Müller 1879), in which an unprofitable model is mimicked by a profitable or unprofitable organism respectively. Neither of these types of mimicry seems to have been reported in insect eggs. One type of egg mimicry that has however been argued to exist in species of several families of Lepidoptera (e.g., Notodontidae, Lymantriidae, Saturniidae, etc.) is one where they look like eggs from which parasitoids have emerged (Hinton 1981). Hinton mentioned that he neglected to collect eggs of Automeris moths in the field because he confused the dark spot on the top of the eggs for emergence holes left by hymenopteran wasps. However, the hypothesis was never tested further with relevant natural enemies, meaning that the existence of such type of mimicry is still debatable, at least in insect eggs. In the case of Automeris eggs (Fig. 3), it seems unlikely that emerged parasitoid mimicry could have evolved given that the sides of the eggs are transparent. This would presumably allow observers to see the orange embryos (which become more visible at the same time as the dark spots appear) still developing in the eggs, and confirm that they have in fact not been parasitized. Further studies, perhaps involving vision modelling of relevant predators, are necessary to properly answer the question.
Fig. 3

Two days old eggs of the saturniid moth Automeris io. These white eggs possess a dark spot on the top as well as a transparent segment on the side of the shell, showing the yellowish-orange color of the developing embryo. Photo by Gary Foster (CC BY-SA 3.0)

Masquerade

In contrast to background-matching camouflage, where a prey is concealed by looking like the substrate it is on, masquerade allows organisms to remain undetected by morphologically and behaviorally mimicking objects found in the environment. However, masquerade differs from mimicry sensu stricto in the sense that the aim of the former is to copy cues while the latter’s is to copy signals (Jamie 2017). Classic examples of masquerade include stick insects looking like twigs, or caterpillars looking like bird feces.

Masquerading as a dew drop

Masquerade has been described in insect eggs, although infrequently. One example comes from a book chapter by Eisner et al. (2002), in which they provided a picture of an “egg of an unidentified coreid bug […] imitative of a dew drop”. From a qualitative stand point, the egg depicted does look like the dew drops next to it, both in terms of shape and color. However, evidence that natural enemies would be fooled by the masquerade is not reported in the text, and no study was cited along with the picture. Thus, conclusions regarding the adaptive significance of this bug’s egg coloration may be somewhat premature.

Masquerading as a seed

Another type of masquerade thought to frequently occur in taxa like moths, stick insects and katydids is seed mimicry (Hinton 1981; Carlberg 1986; Compton and Ware 1991). Insects thought to engage in egg-seed masquerade produce shells that share not only the color, shape and texture, but also special features of the seeds produced by their host plants (Hinton 1981). By looking like seeds, eggs seem to evade predation by insectivorous predators (Carlberg 1986). Yet, seeds are rich in nutrients and are integrated in the diet of numerous herbivorous taxa, both vertebrate and invertebrate. It seems counterintuitive that there is an advantage for eggs to look like an alternative palatable food source: they should be eaten by phytophagous instead of zoophagous organisms. This however may be the key to understand seed masquerade. Hoffmeyer (1970) showed that not only are masquerading eggs unharmed by the digestive system of birds feeding on them, their ingestion also allows for dispersal of the offspring. Thus, seed masquerade provides protection against insectivorous predators and allows for distribution throughout the environment by granivorous herbivores.

Birds are not the only organisms allowing for egg dispersion: ants do it too (Compton and Ware 1991). Multiple species of Formicidae feed on seeds, and are attracted to them thanks to special structures called elaiosomes (Beattie 1985, cited in Compton and Ware 1991). As far as we know, close to half of all subfamilies of Phasmatidae produce eggs that look like plant seeds, but also harbor a capitulum (Clark 1976). These capitula look very much like elaiosomes, and evidence suggests that their presence allows for egg capture by ants and later their dispersal (Compton and Ware 1991). The eggs are brought to the ant nest where the capitula will be fed upon, benefiting the ant and leaving the eggs themselves intact and safe until hatching. Once hatched, the nymphs are left alone by the ants (Compton and Ware 1991) thanks to various adaptations such as ant “mimicry” (Carlberg 1986). It is unclear whether the seed-like color pattern on the eggs plays a role in eliciting myrmecochory, or if ants are only attracted to them by the capitula. The egg coloration itself may only allow for reduction of attacks by natural enemies; future work is required to tease apart the roles of colors and capitula in ant attraction.

Masquerading as a plant organ

Aside from seeds, the eggs of several species from various Lepidopteran taxa tend to resemble other plant organs (Hinton 1981). Some geometrid and nymphalid species lay their eggs on top of each other as to form egg strings, reminiscent of broken tendrils from their host plant. No hypotheses regarding the adaptive significance of this egg-tendril comparison were provided, but a valid one would be that predators regard the eggs as unpalatable plant material and do not attack them. This remains to be tested. Hinton (1981) also mentioned that the eggs of Cerura spp. (Notodontidae) closely resemble the galls formed by other insects on their shared willow and poplar host plants. In addition to their visual similarities, both eggs and galls are found on the upper surface of leaves. It has been hinted that the eggs avoid predation by looking like the galls, but also are probably safe from gall-feeding organisms by possessing spots mimicking exit holes left by gall-producing parasites. However, experimental data are still required to confirm or reject the masquerade hypothesis.

Photoprotection

The reason why some pigments appear black to our eyes is that they absorb most of the wavelengths of the visible spectrum. Those pigments, including melanin, tend to also absorb wavelengths in the ultraviolet range of the spectrum, which can cause damage to DNA (Cadet et al. 2005). UV-protecting egg pigmentation seems to only have been investigated in one insect species: the predacious stink bug Podisus maculiventris (Say, 1832). This species is known to produce polymorphic eggs; each female can selectively apply pigment to the eggs, which can range from pale yellowish-white to dark-brown/black, depending on environmental cues (Abram et al. 2015). Interestingly, pale eggs are usually laid on the underside of leaves while dark eggs tend to be found on leaf tops (Abram et al. 2015) (Fig. 4). This dichotomy has been hypothesized to exist because of heterogeneous solar radiation intensities in the environment. In other words, UV-absorbing pigmentation is necessary on leaf tops as eggs laid there would be exposed to harmful solar radiation, while pale eggs would be safe on the bottom because of UV-absorbent pigments in leaves (Gutschick 1999). Abram et al. (2015) sought to test that hypothesis and found that darker eggs had a higher probability of surviving prolonged exposure to UV radiation than pale eggs, especially at higher intensities. As a case of extended phenotype, parasitoid wasps attacking P. maculiventris eggs also benefit from the photoprotective pigment in question (Gaudreau et al. 2017), which surprisingly is not melanin and has yet to be identified (Abram et al. 2015).
Fig. 4

Eggs of the stink bug Podisus maculiventris. Pale eggs (left) are laid on leaf undersides while dark eggs (right) are laid on leaf tops. Photos by Leslie Abram (with permissions)

The obvious question left unanswered was: why evolve egg pigmentation in the first place? Why not always lay pale eggs on leaf undersides, thus reducing the risk of UV exposure to a minimum while avoiding a potential cost of egg pigmentation? In a follow-up study, Torres-Campos et al. (2016) carried out a field experiment to look at the fate of eggs displaying the whole range of pigmentation, artificially placed on either sides of leaves. Their main finding was that eggs were attacked significantly more often on leaf undersides by predators (but not parasitoids) than on leaf tops, regardless of egg color. In addition, the researchers also found that egg pigmentation does not provide camouflage, but can slightly reduce development time through thermoregulation. Altogether, these results suggest that female P. maculiventris first oviposited on leaf tops as a way to reduce predation risk, leading to the evolution of egg pigmentation in order to survive higher UV radiation intensities on the new oviposition substrate. Torres-Campos et al. (2016) also hypothesized that the selectivity of egg pigmentation is a way to optimize the degree of pigment application and avoid wasting resources to pigment eggs in microenvironments where protection is not required, but their results on resource-limited pigment production were not conclusive. It should be noted that, although P. maculiventris was the only species studied for its selective egg pigmentation, other species from various genera of the Asopinae (e.g., Stiretrus and Zicrona) also seem to possess selective egg pigmentation (Guerra-Grenier, personal observations).

Water retention

Aside from its well-known properties for thermoregulation and photoprotection, melanin can also play a role in water retention. For example, the caterpillars of a geometrid moth vary in their degree of body melanization in response to risk of desiccation in the environment, where melanic larvae develop better in dry environments than non-melanic conspecifics (Välimäki et al. 2015). Such a function for egg melanism has also been described in mosquitoes (Farnesi et al. 2017). In their recent paper, Farnesi et al. (2017) discuss the relationship between the degree of eggshell melanization and resistance to desiccation. They used three species of Culicidae from three different genera, producing pale, grayish and dark eggs respectively. They showed that the probability of hatching increased with denser melanin cover, more so in dryer versus humid environments. Their next step was to measure the effect of melanin on desiccation of eggs of Anopheles quadrimaculatus Meigen, 1818 using two different strains: a wild, dark-brown type and a mutant, gold type. Eggs of the wild type were more viable in a dry environment than eggs of the mutant type, providing evidence that melanization plays a key role in water balance by eggshells.

Areas of future work

After a review of the existing literature on adaptive coloration in insect eggs, two conclusions can be made: (1) the diversity of defensive functions played by egg color, both against biotic and abiotic threats, seems high and is probably underestimated, but (2) many of these functions are still hypothetical and have not yet been experimentally tested. There is a need for empirical studies across the board, especially for cryptic and aposematic egg colorations. Green eggs laid on leaves are common in several orders of insects such as Lepidoptera and Hemiptera, and background-matching camouflage is the most likely explanation for such phenotypes. Toxic eggs with conspicuous orange-red colorations might, on the other hand, be aposematic, but associative learning between color and toxicity by predators should be established before concluding so.

Future studies should therefore aim at quantifying whether relevant egg predators (e.g., ladybugs, lacewing larvae, ants, etc.) and parasitoids can perceive a contrast between egg colors and background colors, using common vision modeling protocols established by other studies in the field of adaptive coloration (e.g., Troscianko and Stevens 2015; Troscianko et al. 2017). Manipulation of egg coloration, using dyes or pastry-based fake eggs, can also allow to test the effect of specific color phenotypes on predatory responses such as latency before detection (for studies on crypsis and masquerade) and associative learning (for studies on aposematic displays and mimicry). In any case, it is of the utmost importance to consider the color vision of the relevant natural enemies and not just that of humans. Birds and insects can frequently perceive ultraviolet wavelengths as colors while humans cannot, meaning that an organism can appear cryptic to us but conspicuous to non-human animals (Briscoe and Chittka 2001; Cronin and Bok 2016).

In the case of mimicry, the ubiquity of Batesian and Müllerian strategies in other life stages makes it likely that such types of mimicry are frequently used by insect eggs. Future work effort should try to uncover the use of such strategies in model systems. For example, Table 1 shows that several chysomelid and coccinellid beetles lay toxic, brightly colored eggs, often yellow-orange. If two or more species co-occur in a given community, it is likely that predators learning to avoid the toxic orange eggs of one species would also be deterred by the similar egg colorations of the other toxic species. This can be true for species co-occurring within a given field, but also on a same host plant (e.g., for eggs of species composing the Müllerian mimicry ring found on milkweed plants).

Future studies on the evolutionary ecology of insect egg coloration should make sure to test for multiple functions provided by the same phenotype. Indeed, color patterns, especially complex ones, often defend organisms against multiple threats (Cuthill et al. 2017). Such is the case for the orange/green markings on the caterpillar of the swallowtail butterfly Papilio machaon L., 1758, cryptic at long range but aposematic at short range (Tullberg et al. 2005), or for the blue/yellow markings on reef fishes used for intra-specific communication at short range but for camouflage at long range (Marshall 2000). Testing for multiple functions of egg color is also important even if some of them are just context-dependent secondary benefits provided by the main adaptive function, like the slight thermoregulatory properties of the photoprotective pigment in P. maculiventris eggs (Torres-Campos et al. 2016). Additionally, phylogenetic analyses would provide us with a better understanding of the evolution of egg coloration in various taxa, by testing whether related species are more likely to have similarly colored eggs. Correlates of egg coloration can also tell us a lot about reproductive strategies and investments. For example, females laying conspicuously colored eggs are more likely to aggregate their offspring compared to those laying eggs that seem to blend in with the background (Stamp 1980). Egg color can also be correlated to egg weight (Wickman and Karlsson 1987) and viability (du Merle and Brunet 1991), depending on the age of the mother at the time of oviposition.

Notes

Acknowledgements

Special thanks go to Thomas N. Sherratt for thorough revisions of every version of the manuscript. I would also like to thank Paul K. Abram, John T. Arnason, Naomi Cappuccino, Andrew Simons, Mark Forbes, Sam Church, Seth Donoughe and Gustavo L. Rezende for helpful discussions and/or comments on the manuscript. This research was supported by a FRQNT postgraduate scholarship.

Compliance with ethical standards

Conflict of interest

The author declares no conflict of interest.

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiologyCarleton UniversityOttawaCanada
  2. 2.Redpath MuseumMcGill UniversityMontrealCanada

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