- Research article
- Open Access
Forewing color pattern in Micropterigidae (Insecta: Lepidoptera): homologies between contrast boundaries, and a revised hypothesis for the origin of symmetry systems
© Schachat and Brown. 2016
Received: 4 February 2016
Accepted: 13 May 2016
Published: 26 May 2016
Despite the great importance of lepidopteran wing patterns in various biological disciplines, homologies between wing pattern elements in different moth and butterfly lineages are still not understood. Among other reasons, this may be due to an incomplete understanding of the relationship between color pattern and wing venation; many individual wing pattern elements have a known relationship with venation, but a framework to unite all wing pattern elements with venation is lacking. Though plesiomorphic wing veins are known to influence color patterning even when not expressed in the adult wing, most studies of wing pattern evolution have focused on derived taxa with a reduced suite of wing veins.
The present study aims to address this gap through an examination of Micropterigidae, a very early-diverged moth family in which all known plesiomorphic lepidopteran veins are expressed in the adult wing. The relationship between wing pattern and venation was examined in 66 species belonging to 9 genera. The relationship between venation and pattern element location, predicted based on moths in the family Tortricidae, holds for Sabatinca just as it does for Micropterix. However, the pattern elements that are lightly colored in Micropterix are dark in Sabatinca, and vice-versa. When plotted onto a hypothetical nymphalid wing in accordance with the relationship between pattern and venation discussed here, the wing pattern of Sabatinca doroxena very closely resembles the nymphalid groundplan.
The color difference in pattern elements between Micropterix and Sabatinca indicates that homologies exist among the contrast boundaries that divide wing pattern elements, and that color itself is not a reliable indicator of homology. The similarity between the wing pattern of Sabatinca doroxena and the nymphalid groundplan suggests that the nymphalid groundplan may have originated from a Sabatinca-like wing pattern subjected to changes in wing shape and reduced expression of venation.
Color pattern in the animal kingdom has been an area of intense study for well over a century . Insects in the order Lepidoptera were the subject of groundbreaking research during the early years of evolutionary biology [2–5] and remain a tremendously popular system for the study of color pattern in a variety of disciplines, ranging from theoretical biology to taxonomy, developmental biology, and ecology [6–9]. However, a disproportionate number of studies of Lepidoptera – such as those cited thus far – have focused on butterflies; the evolutionary history of wing pattern in microlepidoptera is still poorly known. Due to this lack of knowledge regarding wing pattern in more early-diverging lineages, it is difficult to extrapolate findings regarding butterfly wing patterns to other lineages of Lepidoptera.
The present study aims to bridge the gap between butterflies and microlepidoptera. Here we report on wing patterns in Sabatinca and other genera in the family Micropterigidae. Recent studies have confirmed that Micropterigidae, along with Agathiphagidae, are the most basal living moths [10, 11]. Due to the basal phylogenetic position of Micropterigidae, commonalities between the wing patterns of butterflies and Sabatinca should be indicative of ancestral states for all Lepidoptera. Comparisons of the wing patterns of Micropterigidae and butterflies can be confounded by the great differences in wing size and shape in these two clades. However, a recent examination of wing pattern in Micropterix, another genus within the Micropterigidae, showed a consistent relationship between wing venation and color pattern . This relationship with wing venation has the potential to facilitate comparisons of wing pattern in various lepidopteran lineages, as homologies among wing veins are far better understood.
In addition to the “wing-margin” model, another predictive model, proposed decades earlier by Hennig Lemche [21, 22] and referred to here as the “vein-fork” model, predicts that the basal edge of each fascia will fall along the points where veins bifurcate. The wing pattern of Micropterix is not consistent with the “vein-fork” model . Genera such as Sabatinca, which have a more complete suite of plesiomorphic wing veins than Micropterix, are excellent candidates for further testing of the wing pattern groundplan proposed based on Micropterix.
The origin of butterfly “symmetry systems”
These two hypotheses are founded on different assumptions. Lemche, after closely studying wing pattern in many families of microlepidoptera, arrived at the assumption that transverse bands are the primitive wing pattern element for Lepidoptera. Nijhout arrived at the assumption that spots, not transverse bands, are the primitive wing pattern element for Lepidoptera, because “[t]he vast majority of Panorpoid and Trichopteroid wing patterns (like those of many primitive Lepidoptera) are in fact made up of irregular spots, and insofar as these groups are sister groups of the Lepidoptera, spotted patterns are most likely to represent the p[r]imitive (plesiomorphic) condition for the Lepidoptera” . However, the connection between trichopteran spotted wing patterns and the plesiomorphic character state for Lepidoptera is not entirely straightforward. In Trichoptera, spots are very small and mainly occur along the wing margin. But in the most basal moths that have spotted wing patterns – Neopseustidae, Hepialidae, and, to a certain extent, Lophocoronidae and Eriocraniidae – spots are much larger and occur throughout the entire wing. Also, in Trichoptera as in all other Panorpoidea aside from Lepidoptera, color pattern is most often associated with the wing membrane, but in Lepidoptera, color pattern rarely occurs on the wing membrane and is nearly always associated with wing scales. The role of gene expression in wing pattern development remains largely unexplored in microlepidoptera and in Trichoptera; theoretically, the same genes could influence the development of color pattern in all cells on the wing, regardless of whether a cell ultimately differentiates into an epithelial cell or a scale. But because color pattern elements on the wings of Trichoptera and Lepidoptera are very different in appearance and occur in different anatomical structures – membrane versus scales – proposed homology of color pattern elements between these two orders remains somewhat dubious.
The two mutually exclusive hypotheses for the origin of symmetry systems rely on conflicting assumptions; a test of these assumptions would be a first step toward rejecting one, or perhaps ultimately both, of these hypotheses. In addition to the primitive state for lepidopteran wing pattern elements, another question must be resolved in order to reconcile microlepidopteran wing pattern with the origin of symmetry systems: the influence of wing venation on wing pattern development. In Lepidoptera with symmetry systems, such as butterflies, certain types of wing pattern elements – such as venous stripes – are unquestionably dependent on venation . Other pattern elements, such as melanic band pattern elements, are not so obviously dependent on venation and may develop even if a species’ typical suite of venation is not expressed in the adult wing . However, observations over many decades have confirmed that plesiomorphic veins can continue to influence the development of butterfly wing pattern elements, such as eyespots, even if the veins are not expressed in the adult wing [24, 30], so the presence of a wing pattern element in the absence of expressed corresponding venation does not necessarily indicate that wing venation is irrelevant to that pattern element. Because many plesiomorphic lepidopteran wing veins are not distinguishable in the adult wings of butterflies and other higher Lepidoptera, either due to fusion or lack of expression, the relationship between venation and color patterning is especially difficult to deduce in these taxa, and has been granted little consideration.
Primitive lepidopteran wing venation
Though we do know with absolute certainty that plesiomorphic wing veins can influence color pattern elements (such as eyespots) even when not expressed, the relevant groundplan of primitive lepidopteran wing venation remains less certain. Because lepidopteran color patterns are unique in that they arise from scales, a reasonable working hypothesis is that the veins with potential to influence the development of color pattern are those that were present in the ancestral lineage in which scales first originated, regardless of whether these primitive scales expressed color. However, identification of this lineage, and the wing veins that it possessed, is hindered by the nature of the lepidopteran fossil record. The timing of the split between Trichoptera and Lepidoptera is unknown; the earliest definitive Trichoptera and Lepidoptera both date to the Mesozoic, but the recent finding of putative caddisfly cases from the early Permian would move this split much farther into the past . Moths have a remarkably poor fossil record  and putative stem-group fossils are plagued by taxonomic uncertainty . In the earliest known fossil of a true moth, Archaeolepis mane, only one branch of the Sc vein is visible [34, 35]. But early-diverging moths such as Micropterigidae overwhelmingly possess a two-branched Sc vein, and because a multi-branched Sc vein is the plesiomorphic character state for ancestral Amphiesmenoptera [16–18], A. mane is highly unlikely to represent the ancestral state for lepidopteran wing venation.
Other Jurassic fossil moths offer limited additional information about ancestral wing venation. New discoveries are very rare , and fossils previously assigned to the extinct trichopteran family Necrotauliidae have been shifted to Lepidoptera on the basis of wing venation – more specifically, a 3-branched medial vein . Unsurprisingly in light of the fact that assignment of Jurassic amphiesmenopteran fossils to Lepidoptera depends largely on similarities with venation in extant moths, the most recent hypothesis for primitive lepidopteran venation  bears a striking resemblance to wing venation in Micropterigidae such as Sabatinca. There is reason to doubt that this hypothesis is complete: it contains a three-branched M vein, as is found in Sabatinca and other Micropterigidae, but the presence of a four-branched M vein in Permotrichoptera [17, 18], Mesozoic caddisflies , extant caddisflies , and the extant lepidopteran family Agathiphagidae  – recently shown to belong to the earliest-diverging branch of Lepidoptera, alongside Micropterigidae [10, 11] – suggests that more veins may need to be added to the reconstruction of primitive moth venation. Given the paucity of data available to inform hypotheses of primitive lepidopteran wing venation, the possibility certainly exists that additional wing veins known from other Amphiesmenoptera may have also been present in early moths, and may therefore continue to influence the development of color patterns in extant Lepidoptera.
Micropterigidae: systematics and wing pattern morphology
Studies of micropterigid wing scales have found that they are always internally “fused” and therefore lack a cavity to hold pigment sacs . Photos and written descriptions show that micropterigid wing scales are often iridescent [39, 42, 43].
Terminology is used as follows. A “wing pattern element” formed by two or more adjacent wing scales of the same color, and can take the form of a spot, band, patch, etc., and the term “band” is used as shorthand for “transverse band,” which is a band that runs more or less between the costal and dorsal margins of the wing. The term “fascia” is rarely used here; this term has recently been subject to varying interpretations regarding wing pattern in Micropterigidae, having been applied to both light bands [43, 44] and to dark bands . The term “band,” as used here, encompasses both interpretations of “fascia.” Similarly, the term “ground color” is avoided here because this term usually signifies the color that covers the greatest amount of wing surface area, but this can vary between very light and very dark brown even among closely related species within the same genus. For the sake of simplicity, the term “color” is applied broadly, to encompass all distinguishable colors, shades, tones, and tints. Therefore, white, silver, blue, brown, and black are discussed as “colors,” and different tints, tones, or shades – for example, light and dark shades of brown – are considered to be separate colors. The use of the term “color” here does not discriminate between structural colors and those derived from pigments. Nomenclature for wing venation (Fig. 1) mainly follows Wootton , with the exception of the humeral vein (“h”). The wing veins referred to with conventional nomenclature are those that are visible in the adult wing of Sabatinca. Schachat and Brown hypothesized that a third branch of Sc, known to be plesiomorphic for Amphiesmenoptera, plays a key role in micropterigid wing pattern; this hypothesized vein is referred to here as “pSc,” for plesiomorphic Sc (Fig. 1). Many species from New Caledonia are referred to here with numbers (“Sabatinca spp. 43, 20, 47, 29, 46, and 11,” etc.); these are the same numbers that were used to refer to undescribed species included in the recent Sabatinca phylogeny .
Forewing pattern in New Zealand Sabatinca
The wing pattern of Sabatinca aemula (Fig. 5h) is similar to that of S. aurella in that the lightest scales form transverse markings that are bordered by the darkest scales on the wing. Two major differences between Sabatinca aemula and S. aurella are immediately apparent: firstly, the wing pattern of S. aemula is not entirely fasciate, as the darkest scales often form spots, and secondly, medium-colored scales straddle alternating veins along the costa of S. aurella but straddle only one vein, h, along the costa of S. aemula. The wing pattern of Sabatinca chrysargyra is broadly similar to that of S. aemula in terms of the positioning of pattern elements relative to veins along the costa, but contains spots of varying sizes instead of any discernible fasciae (Fig. 5i). In Sabatinca chrysargyra, unlike S. aurella and S. aemula, the darkest pattern elements are spots and do not occur adjacent to the lightest pattern elements.
The wing patterns of other Sabatinca species in the “chrysargyra group” do not lend themselves as obviously to comparison with the wing pattern of S. aurella, and are discussed in order of complexity as follows. In Sabatinca ianthina, the predominance of dark wing pattern elements is such that dark scales straddle every single vein along the costa (Fig. 5f). Sabatinca quadrijuga also has a wing pattern that consists overwhelmingly of dark scales; certain lighter wing pattern elements do straddle veins at the costa, but this occurs only at the h and Sc veins (Fig. 5a). Sabatinca caustica and S. chalcophanes share a banding pattern in which fasciae converge toward the middle of the dorsum (Fig. 5b, c). In both species, wing pattern is quite variable at the costal margin of the wing and all veins that reach the costa, including the humeral vein, are surrounded by dark scales in at least some specimens.
Forewing pattern in New Caledonia Sabatinca
The two New Caledonian species shown to be most basal, Sabatinca spp. 33 and 4, have somewhat fasciate wing patterns consisting of three colors. In Sabatinca sp. 33 (Fig. 6c), only two the lightest and darkest colors reach the costa. The darkest brown straddles the humeral vein, and then alternating veins: Sc1, R1a, Rs1, and sometimes Rs3. In Sabatinca sp. 4, all three colors reach the costa (Fig. 6d). The main transverse bands alternate between light and medium brown, with small dark brown spots and bands appearing at the basal edge of the light bands.
Forewing pattern in other Micropterigidae
In Nannopterix choreutes (Fig. 11f), a dark band abuts the basal edge of Sc1 at the costa and a medium band straddles Rs2. In Aureopterix micans (Fig. 11g), dark bands straddle Sc1, Sc2, and Rs1 at the costa. Sometimes the band that straddles Rs1 also straddles Rs2 and Rs3, and, less often, R1b. In Aureopterix sterops (Fig. 11h), dark bands consistently straddle Sc2 and Rs2 at the costa; the band that straddles Rs2 sometimes extends to Rs1 and R1b. In Zealandopterix zonodoxa (Fig. 11i), the only light wing pattern element that consistently reaches the costal margin of the wing is a small spot that occurs at the apex and does not straddle any veins; in some specimens, one light band occurs at the “pSc” area of the costa between Sc1 and Sc2 and another light band abuts Rs1.
A revised hypothesis for the origin of symmetry systems
The wing patterns of certain Sabatinca species illustrate a straightforward mechanism though which symmetry systems could have originated. This observation has led us to revise Lemche’s original “split-band” hypothesis for the origin of symmetry systems so that it includes aspects of the “wing-margin” model.
Because micropterigid and nymphalid wings are so different in size, shape, and venation, the wing pattern of Sabatinca doroxena could be projected onto a nymphalid wing in any number of ways. However, the exacting predictions of the “wing-margin” model allow this to occur in only one way. In Sabatinca doroxena, the basal half of the nearly-split band that straddles the humeral vein is comprised of a single color, the apical half is bisected by a lighter color, and one more band – again, bisected by a lighter color – reaches the margin of the wing basal to the terminal branch of the subcostal vein. According to the nymphalid groundplan, three such bands – a unicolorous band at the base of the wing, followed by two symmetry systems – reach the costa before Sc terminates. On the wing of Sabatinca doroxena, three additional concentric, two-color bands occur between the terminal branch of Sc and the terminal branch of Rs. However, because Sc terminates so close to the apex in Nymphalidae, the nymphalid wing simply does not contain sufficient space for three symmetry systems beyond Sc – much in the same way that the pattern element straddling Rs4 in Micropterix originates along the costa and develops into a band, and is called the “terminal fascia,” but the pattern element straddling this same vein in Tortricidae does not occur along the costa of the wing and can only exist as a spot . And so in Nymphalidae, there is only space for one symmetry system beyond Sc; two very thin unicolorous bands appear between this symmetry system and the termen of the wing, such that the total number of wing pattern elements beyond Sc is the same in Nymphalidae as it is in Sabatinca doroxena; the fact that the two terminal wing pattern elements in Nymphalidae do not resemble those in Sabatinca doroxena is a necessity according to the “wing-margin” model due to differences in wing shape between these two taxa (Fig. 14).
Most features of the nymphalid groundplan have a corresponding pattern element in Sabatinca doroxena and S. aurella. The only nymphalid groundplan features not accounted for in the wing patterns of S. doroxena and S. aurella are the discal spot (“DS” or “DI”) and the distal portion of the distal band of the central symmetry system (“dBC”), a feature that is illustrated as a discrete entity by some authors  but treated simply as the distal margin of the central symmetry system by other authors . The discal spot could have arisen if the central symmetry system, corresponding to the pattern element that located in the “pSc” area of the wing in Sabatinca, originated from a band that hypertrophied not once but twice. A discrete, visible “dBC” pattern element, marked with an asterisk (Fig. 14c), could have originated if a very thin band, akin to the silvery striae in Tortricidae, appeared alongside the central symmetry system but later became decoupled from it and moved toward the apex of the wing. But again, “dBC” is considered to simply represent the distal margin of the central symmetry system.
The resemblance of certain Sabatinca wing patterns to the nymphalid groundplan suggests a revised version of Lemche’s “split-band” hypothesis for the origin of symmetry systems, in which symmetry systems originate from one-color bands that are bisected by another color and become concentric – but the location of these bands is constrained by veins at the costa, as postulated by the “wing-margin” model, instead of the points where veins bifurcate. This novel combination of two compatible concepts that had previously been discussed in isolation – the “wing-margin” model for band location and the “split-band” hypothesis for the origin of symmetry systems – fits the nymphalid groundplan very closely. Because the wing patterns of Sabatinca doroxena and S. aurella so closely match the nymphalid groundplan, the revised hypothesis presented here is currently better supported by empirical data than Lemche’s original “split-band” hypothesis and Nijhout's “fused-spot” hypothesis that had been proposed previously.
Comparison with developmental mechanisms known from other Lepidoptera
The earliest studies of wing pattern evolution in Lepidoptera were based primarily on morphology, with preliminary phylogenetic context [47–49]. The first rigorous examination of wing pattern morphology in the context of phylogeny is over a century old  and is roughly contemporaneous with influential studies of other aspects of lepidopteran morphology . In the wake of the publication of the nymphalid groundplan [24, 25], comparative morphology was a popular area of study that overlapped heavily with early experimental work on heredity [21, 22, 52–54]. During the current era, morphological insights continue to inform our understanding of the systematics of Lepidoptera [55, 56] and of the nymphalid groundplan . Wing pattern homologies are designated through a combination of developmental, phylogenetic, and morphological data , and morphological data continue to shed light on the developmental genetics of color pattern, particularly when combined with phylogeny . Developmental studies of wing pattern in Micropterigidae are not possible at present because no lab colony has been established, despite years of effort. However, current knowledge of the genetic underpinnings of wing pattern in macrolepidoptera and other panorpoid insects includes developmental mechanisms that may be relevant to Micropterigidae.
Expression of the developmental morphogen wingless precedes the development of wing pattern elements in many families of Lepidoptera , and also precedes the development of spots that are associated with venation in certain species of Drosophila . In various macrolepidoptera, wingless is implicated in the development of two elements of the nymphalid groundplan [46, 59]: first, the discal spot (“Discalis I”) a wing pattern element that terminates near the costal margin of the wing and is associated with vein forks, but which does not correspond to any wing pattern element in Micropterigidae (Fig. 14); and second, the basal symmetry system (sensu Otaki ), also called “Discalis II,” which corresponds with the pattern element that terminates along the costal margin basal to Sc1 in Sabatinca doroxena and S. aurella.
The gene product WntA is involved with the development of various symmetry systems on butterfly wings, and is sufficiently well understood that its expression can be used to identify pattern homologies in situations where morphology is confusing or unclear . In theory, the wing patterns of alternating light and dark stripes seen in Micropterigidae could develop as a result of the expression of wingless and WntA. Certain existing studies that use the nymphalid groundplan as a starting point have included various lineages of moths ; the results presented here can be used to guide the identification of nymphalid groundplan pattern elements in microlepidoptera, facilitating further taxonomic expansion of developmental studies.
Ancestral states and the nature of wing pattern homology
A comparison of wing pattern in Micropterix and Sabatinca shows that the color of each pattern element can confound identification of homologies. The contrast boundaries that divide pattern elements, as opposed to the colors of pattern elements themselves, are the best indicators of homology.
The number of primitive fasciae in Lepidoptera
Our results suggest that the primitive number of fasciae in Lepidoptera is less than seven. Wing patterns with seven or more fasciae have likely originated convergently in many lineages, perhaps evolving from the spots found in certain derived species of Sabatinca.
Though the “wing-margin” and “vein-fork” models share the assumption that transverse bands are the primitive wing pattern element for Lepidoptera, the two models differ in that the “vein-fork” model proposed a primitive groundplan with seven dark bands whereas the “wing-margin” proposes a primitive groundplan with either five or six dark bands, depending on whether Rs4 terminates along the costa. Sabatinca doroxena has a wing pattern of five dark bands that is entirely consistent with the “wing-margin” model’s prediction about the location of contrast boundaries (Fig. 5d). The band that straddles the humeral vein is part of a V-shaped pattern element that could have originated from a fasciate wing pattern in one of two ways: either two dark bands became confluent at the dorsal margin, or one dark band was split by a light pattern element that runs from the costa nearly to the dorsum. In Sabatinca aurella, this putative split is complete: the two apparent dark bands appear basal to Sc1 along the costa, with one straddling the humeral vein and one that does not straddle any vein (Fig. 5e). There are two simple explanations for this apparent split from one dark band into two. The first is that only one dark band occurred basal to Sc1 in ancestral Sabatinca, with this band nearly split in S. doroxena, and apparently completely split into two bands in S. aurella – though these features in both species are derived from a single primitive band. The second explanation is that two dark bands occurred basal to Sc1 in ancestral Sabatinca, which would require an additional two plesiomorphic branches of Sc – completely unknown from Trichoptera as well as Lepidoptera – to influence the development of wing pattern in extant Lepidoptera. The first explanation, of one primitive band that appears to split into two, is far more conservative in that it does not require the presence of plesiomorphic veins unknown from crown Amphiesmenoptera (the clade that includes all living moths and caddisflies), and is arguably also the more plausible of the two explanations given that multiple bands preceding Sc1 are not known from any micropterigid genus besides Sabatinca.
Implications for Lemche’s “vein-fork” model
Though micropterigid wing patterns overwhelmingly do not conform to Lemche’s “vein-fork” model, a few species do offer insight into the processes that inspired the model.
Lemche’s “vein-fork” model for homology between wing pattern elements was originally based on observations of the location of spots on the wings of Pyralidae and Noctuidae . Lemche found that spots often occurred at the points where veins bifurcate, and he extrapolated this observation from spots to fasciae, predicting that the basal edges of fasciae should also lie along points where veins bifurcate. This model therefore implies that fasciae and spots are homologous; because Lemche hypothesized that fasciae are the primitive wing pattern elements for Lepidoptera , one would expect that the spots in Pyralidae, Noctuidae, and many other moths to have arisen via incomplete expression of bands.
The “vein-fork” model initially appeared to be irrelevant to Micropterigidae, and therefore quite possibly of limited relevance to the evolution of wing pattern in Lepidoptera, because the model does not predict the location of fasciae in Micropterix . The data presented here show that the model is of similarly limited utility for predicting the location of fasciae on the wings of other micropterigid taxa. However, in two Sabatinca species that appear to be distantly related – S. demissa (Fig. 6b) and S. sp. 6 (Fig. 7e) – prominent large, dark spots occur at many of the points where veins reach the wing margin and also at the point where the M vein bifurcates. In Sabatinca demissa, additional dark spots occur where Rs and CuA bifurcate; many more spots occur elsewhere on the wing, but are either much smaller or much lighter in color than those that occur where veins meet the wing margin and where M bifurcates. It is striking that the largest dark spots appear in the same locations relative to venation in both Sabatinca sp. 6 and S. demissa, because these two species’ color patterns are otherwise dissimilar: S. sp. 6 has large spots and bands that are very light in color whereas S. demissa has small, medium-brown spots against a very light ground color. Because prominent spots at the bifurcation of M are rare in Micropterigidae and have likely originated independently twice in Sabatinca alone (Fig. 17), it appears that Lemche erred in assuming that the spots in Pyralidae and Noctuidae are homologous and ancestral within and beyond the Lepidoptera . The origination of such spots at vein bifurcations may well be a real phenomenon, but appears to have occurred convergently in various lepidopteran lineages and would therefore be homoplastic.
Wing patterns with two colors
Both models put forth to explain wing pattern homology in microlepidoptera – the “wing-margin” model and the “vein-fork” model – assume a wing pattern that, at a first approximation, is comprised of one relatively light color and one relatively dark color. Though both models are based on taxa whose wing patterns include more than two colors, evaluation of these models is most straightforward for taxa whose wing patterns include only two colors. Six of the genera examined here – Austromartyria, Hypomartyria, Aureopterix, Zealandopterix, Tasmantrix, and Epimartyria – have wing patterns with only one light and one dark shade of brown, and all of these wing patterns are consistent with the “wing-margin” model. However, none of these genera provide as robust a test of the model as Micropterix because none have more than four pairs of alternating light and dark bands.
Other than Micropterix, Epimartyria (Fig. 13) is the only genus in the Laurasian, Northern Hemisphere clade whose wing pattern includes more than one color (Fig. 16). The wing patterns of both E. bimaculella and E. pardella could be said to be consistent with the “wing-margin” model, in that the single light pattern element at the costa straddles only one vein. However, because so few differentiated pattern elements occur on the wing of Epimartyria, this genus does not provide any additional insight into the applicability of the “wing-margin” model to Micropterigidae.
The wing patterns of all taxa in the “Australian group” are consistent with the “wing-margin” model as observed in Micropterix. The only light band that reaches the costa in most Tasmantrix species (Fig. 12) corresponds to the interfascial area that separates the subbasal and median fasciae in Micropterix (Fig. 1), and the light band that reaches the costa in T. lunaris and T. tasmaniensis corresponds to the interfascial area between the median and postmedian fasciae in Micropterix, with additional lack of expression of the postmedian fascia at R1b in T. tasmaniensis. The wing pattern of Zealandopterix (Fig. 11i) is dominated by dark pattern elements and consists of a small spot at the base of the wing that does not reach the costa, a smaller spot at the wing apex that does not straddle any veins, a light band that reaches the “pSc” area of the costa that separates the subbasal and median fasciae as in Tasmantrix (Fig. 12) and Micropterix (Fig. 1), and a light band that straddles Rs1, corresponding to the interfascial area that separates the postmedian and preterminal fasciae in Micropterix. Wing pattern in Tasmantrix and Zealandopterix is therefore consistent with the “wing-margin” model with confluence of fasciae due to suffusion of interfascial areas, plus with the addition of small light spots between fasciae. In contrast to the other genera in the “Australian group,” Aureopterix (Fig. 11g, h) has a wing pattern dominated by light pattern elements. Nevertheless, the wing pattern of Aureopterix micans (Fig. 11g) is broadly consistent with the Micropterix groundplan (Fig. 1): dark bands straddle Sc1 and Sc2 exactly as predicted by the “wing-margin” model, corresponding to the subbasal and median fasciae; R1b is sometimes straddled by a dark band, corresponding to the postmedian fascia; and Rs2 is straddled by a dark band corresponding to the preterminal fascia, which has become confluent with the postmedian fascia. The wing pattern of Aureopterix micans can therefore be derived from the “wing-margin” model through lack of expression of the basal fascia and confluence of the postmedian and preterminal fasciae. The wing pattern of Aureopterix sterops (Fig. 11h) is very similar, except that the basal fascia is partially expressed, the subbasal fascia does not straddle Sc1 at the costa due to incomplete lack of expression, and the postmedian and preterminal fasciae are not confluent as frequently. Between Aureopterix micans and A. sterops, all fasciae and interfascial areas predicted by the “wing-margin” model are present with the sole exception of the terminal fascia, which is absent by necessity because Rs4 does not terminate along the costa in Aureopterix.
In the two “southern sabatincoid” genera whose wing patterns contain two colors, Austromartyria and Hypomartyria (Fig. 11a, b), the only veins ever straddled by light bands are Sc1, Sc2, and R1b. These three veins form an alternating series, as they are interspersed between h, “pSc,” R1a, and Rs1, and so at first glance the southern sabatincoid wing patterns appear to be consistent with the “wing-margin” model. However, the model predicts that these veins should be straddled by dark, not light, bands (Fig. 1). The contrast boundaries between wing pattern elements in Austromartyria and Hypomartyria are consistent with those predicted by the “wing-margin” model, but the colors of these pattern elements are not – just as in Sabatinca doroxena and S. aurella (Fig. 15). Because Austromartyria, Hypomartyria, and Sabatinca form a single clade (Fig. 16), it appears that the common ancestor of all Micropterigidae had a wing pattern that conforms to the “wing-margin” model (Fig. 1) in terms of both contrast boundary location and pattern element color – as seen in Micropterix, Tasmantrix, Zealandopterix, and Aureopterix – and that the common ancestor of Austromartyria, Hypomartyria, and Sabatinca had a wing pattern in which the dark pattern element of Micropterix became light, and vice-versa.
Only three of the Sabatinca species examined have wing patterns with just two colors: S. quadrijuga (Fig. 5a), S. ianthina (Fig. 5f), and S. sp. 36 (Fig. 7b). The only light wing pattern elements that reach the costa in Sabatinca quadrijuga straddle Sc1 and Sc2, just as in Austromartyria (Fig. 11a); no light wing patterns straddle any veins along the costa of S. ianthina or S. sp. 36. The latter two species, though phylogenetically and geographically distant from each other (Fig. 17), have very similar wing patterns: an overwhelmingly dark wing with very light pattern elements occurring basal to the humeral vein, in the “pSc” area, between R1a and R1b, straddling or very close to Rs4, and between M3 and CuA1; S. ianthina also has a light band between Rs2 and Rs3 and small light spots between M1 and M2. This wing pattern could be derived from the Micropterix groundplan through complete suffusion of various interfascial areas, and incomplete suffusion of all others; both complete and incomplete suffusion of interfascial areas have been observed in various Micropterix species . The small light bands along the costa in these two species correspond to the Micropterix interfascial area that straddles “pSc” and the Micropterix interfascial area that straddles R1a, with incomplete suffusion adjacent to the median fascia. The additional light band on the wing of Sabatinca ianthina corresponds to the interfascial area that straddles Rs3 in Micropterix (Fig. 1), with incomplete suffusion adjacent to the terminal fascia. The light band that straddles Rs4 in many Sabatinca sp. 36 specimens could be attributed to lack of expression of the terminal fascia along the dorsum and incomplete suffusion of the adjacent interfascial area along the costa. Both of these groundplan modifications have been observed in M. rothenbachii, though not in the same specimen . Because few Sabatinca species have wing patterns comprised of only two colors, and because these wing patterns are characterized by extensive suffusion of interfascial areas, this genus adds little to our understanding of micropterigid wing patterns that are comprised strictly of one light shade and one dark shade of brown.
Wing patterns with three or more colors
Wing patterns include three or more colors in Nannopterix, Agrionympha, and the vast majority of Sabatinca species. In Nannopterix choreutes (Fig. 11f), light scales straddle all veins at the costa except for Rs2 and so no firm conclusions can be drawn regarding the “wing-margin” model, or homology in any other sense. In Agrionympha (Fig. 11c-e), light bands are bordered by very dark, thin bands. Among various other possible mechanisms, these very dark bands could have arisen in the manner predicted by Lemche’s “split-band” hypothesis, with each pair of dark bands originating from a single, ancestral dark band that was bisected by a very light band. In the three Agrionympha species examined here, a light band and the two very dark bands that border it all fall within the “pSc” region, occasionally abutting Sc1 but never straddling either of the Sc veins expressed in the adult wing; because all two-colored micropterigid wing patterns are consistent with the “wing-margin” model, which predicts a single wing pattern element in the “pSc” are between Sc1 and Sc2, this suggests that each light band, plus the two very dark bands that border it, function together as a single wing pattern element. The three Agrionympha species examined have a another “split-band”-type wing pattern element at R1, but because this pattern element straddles different veins in different taxa – R1b in A. capensis and A. fuscoapicella and R1a in A. sagittella – it is difficult to determine how this pattern element, and therefore Agrionympha wing patterns as a whole, might relate to the “wing-margin” model.
In Sabatinca, the relationships between wing pattern elements of different colors seem to vary greatly among species. For example, in the chrysargyra group (Fig. 5) – a small, well-supported clade – Sabatinca doroxena and S. aurella have fasciate wing patterns in which the one or two most basal dark bands are of a single color, but all others are bisected by a very light color (Fig. 5d, e). These wing patterns essentially provide an illustration of the “split-band” hypothesis, because the basal bands conform exactly to Lemche’s hypothesized ancestral state for microlepidopteran wing pattern and the others conform exactly to Lemche’s hypothesized incipient symmetry systems. A few other Sabatinca species, such as S. lucilia (Fig. 4c), have wing pattern elements that somewhat resemble the “split-band,” but not as unambiguously so. In Sabatinca caustica and S. chalcophanes (Fig. 5b, c), the darkest wing pattern elements occur only at the costal and dorsal wing margins and are connected by medium-brown bands. In Sabatinca chrysargyra (Fig. 5i), the darkest pattern elements are small spots that straddle veins at the wing margin and the lightest pattern elements are much larger bands that do not straddle veins.
In the incongruella group, three-color wing patterns are even more varied. Sabatinca demissa (Fig. 6b) has large, dark spots at the points where veins reach the costa or bifurcate, and small, light spots elsewhere. In Sabatinca sp. 33 (Fig. 6c), only the lightest and darkest wing pattern elements reach the costa, with the exception of Rs3 in some specimens. Sabatinca sp. 6 (Fig. 7e) and the distantly related S. sp. 12 (Fig. 9a) have color patterns very similar to that of S. chrysargyra (Fig. 5i). Many Sabatinca species from New Caledonia have wing patterns somewhat similar to the “split-band”-type patterns of Sabatinca doroxena and S. aurella from New Zealand, but the thin, dark bands of S. doroxena and S. aurella often do not appear as bands at all in the New Caledonian species and instead are either broken up into small spots or are absent altogether, particularly at the apical, or distal, margin of each light band. However, the relationship between patterning and venation differs markedly between the “split-band”-type Sabatinca species of New Zealand and New Caledonia: whereas the “split-band”-type pattern elements straddle alternating veins along the costa in the New Zealand species (Fig. 5d, e) and in Sabatinca sp. 31 from New Caledonia (Fig. 7a), it is common for every single vein along the costa to be surrounded or abutted by a “split-band”-type pattern element in New Caledonian species (Figs. 8b-g and 10b, h).
Sabatinca sp. 37 (Fig. 9e) has a wing pattern of only two colors except at the apical area. Its wing pattern is not exactly fasciate – if this wing pattern is indeed derived from an ancestral fasciate pattern, the edges of the fasciae have become rather sinusoidal, creating a reticulate pattern comprised of elements that simultaneously resemble both fasciae and spots. However, these sinusoidal fasciae do straddle alternating veins along the costa: the area basal to Sc1, the “pSc” area, R1a, and Rs1. (Rs3 is straddled by a light band that also straddles both Rs2 and Rs4.) Because the various colors on the wing of Sabatinca sp. 37 are limited to constrained to small portions of the wing, potential relevance to the “wing-margin” model may be easier to deduce.
In summary, third and fourth colors in Sabatinca wing patterns seem to have originated independently multiple times and through a variety of mechanisms, often obscuring homologies with more straightforward pattern elements seen on the wings of other micropterigid genera with wing patterns comprised of only two colors, such as Tasmantrix, Austromartyria, and Micropterix. In Sabatinca sp. 37 the four colors in the wing pattern are largely confined to specific areas along the proximo-distal axis and in S. sp. 33 colors are confined to specific areas along the anterior-posterior axis, but in all other species, different colors are dispersed throughout the wing. In Sabatinca demissa, the color of a spot corresponds with its proximity to the points where veins bifurcate and terminate. In Sabatinca sp. 6, the darkest spots along the costal margin always straddle veins and the lightest spots never do. In Sabatinca doroxena and S. aurella, the lightest color on a wing, either beige or white, seems to have originated within the central areas of the dark brown bands. In various putative spider mimics, blue and light brown bands are adjacent to each other and may have originated when one band split into two, losing its self-symmetry. Many species from New Caledonia have transverse light bands surrounded by dark bands or spots on both sides; there is a consistent relationship between venation and both of the band colors – light bands always straddle Sc1 and Sc2, and a dark band always straddles R1a – suggesting that both of these colors, whether they arose from the hypertrophy seen in Sabatinca doroxena and S. aurella or by some other mechanism, are developmentally individuated.
From an examination of micropterigid wing patterns that are comprised of two colors, it appears that the ancestral state for this family – and therefore quite possibly for the order Lepidoptera – is a wing pattern of alternating light and dark bands, with each band straddling one vein along the costa. This ancestral state conforms to the predictions of the “wing-margin” model, originally based on Tortricidae [13, 14]. However, a comparison of the wing patterns of Micropterix with Sabatinca doroxena and S. aurella shows that the “wing-margin” correctly predicts the location of transverse bands and the contrast boundaries between them, but cannot predict which series of bands will be light brown and which will be dark brown. The wing pattern elements of Sabatinca doroxena and S. aurella – simple bands of a single dark color, and two-color bands in which dark scales surround a central light area – illustrate both stages of “split-band” symmetry system formation hypothesized by Lemche , thus strongly supporting his hypothesis that symmetry systems originated when dark bands were bisected, or hypertrophied, by light bands. When the wing pattern of Sabatinca doroxena is plotted on to a nymphalid wing following the constraints proposed by the “wing-margin” model, the resulting hypothetical wing pattern very strongly resembles the nymphalid groundplan. Because the “wing-margin” model correctly predicts the location of wing pattern elements in distantly related lepidopteran lineages (Micropterigidae, Tortricidae), and, in combination with the “split-band” hypothesis, can predict the nymphalid groundplan based on wing pattern in Sabatinca, the “wing-margin” model and the “split-band” hypothesis appear to have great potential to explain wing pattern diversity in the order Lepidoptera.
The specimens examined for this study are held in the Australian National Insect Collection in Canberra, Australia; Victoria University in Wellington, New Zealand; and the Smithsonian Institution in Washington DC, USA. Only forewings were examined, because hindwings have very light scales of only one color. A total of 918 wings were examined, which may have included one or both forewings from a given specimen – the only wings that were excluded are those in which the relationship between venation and patterning cannot be deduced because the scales are worn off or the wing is broken. These 918 wings represent 66 species and 9 genera of Micropterigidae. Taxa were selected to match those sampled in the existing preliminary micropterigid phylogeny . Sampling differences between the preliminary phylogeny and the present study are as follows: Micropterix was not included here because this genus has already been examined ; Sabatinca spp. 5b, 49, and 50 were not included here because these species are only known from specimens preserved in ethanol; and Epimartyria auricrinella and the genera Paramartyria, Palaeomicroides, Issikiomartyria, Kurokopteryx, and Neomicropteryx were not included here because these species’ wings are of only a single color, a dark brown similar to the color of dark bands in Micropterix [20, 40]. Additional species belonging to the genera Epimartyria (E. bimaculella) and Tasmantrix (T. calliplaca, T. lunaris, T. nigrocornis, T. phalaros, and T. tasmaniensis), and species representing the additional genera Agrionympha (A. capensis, A. fuscoapicella, and A. sagittella) and Nannopterix (N. choreutes) were included here, despite being absent from the preliminary phylogeny, because specimens were available and because the affinities of these additional genera have already been discussed in the literature [42, 61].
The methods used here to examine wing pattern morphology parallel those developed by Schachat and Brown  and are as follows: For each species, one forewing from one specimen was selected to form the basis of the illustration of that species’ wing pattern. The wings selected were those that had intact color pattern, minimal overlap between the forewing and hindwing, and minimal overlap between the wing and the small block holding the minuten pin. This allowed maximum light to shine through the backlit wing. Scaled wings, instead of cleared wings, were examined in order to observe the precise relationship between color pattern and venation. Micropterigid wings are thinly scaled, and the venation becomes visible when specimens are lit from below using a microscope stage light. The observed wing venation was confirmed by examination of published illustrations of wing venation [40, 61, 62] and by examination of a wing slide prepared by Don Davis and Jean-Francois Landry and held at the USNM for Epimartyria bimaculella, and by examination of wing slides prepared by George Gibbs and held at Victoria University for all other species; for the 7 species for which wing slides are not available (Agrionympha capensis, A. sagittella, A. fuscoapicella, Sabatinca viettei, and S. spp. 36, 39, and 43;), the wing slide of a sister species was examined for Sabatinca and published illustrations were consulted for Agrionympha .
To verify that the illustrations fully represent the species to which they correspond, a total of up to 20 forewings were examined under a light stereomicroscope. (Results are discussed primarily in terms of wings instead of specimens because, in a few cases, only one forewing could be examined per specimen due to wear, due to the angle at which the specimen had been pinned, or because one wing had been removed to make a wing slide. Furthermore, a number of specimens have color patterns that varied between the two forewings.) Variations were noted at all locations along the costa where veins terminate, with the frequent exception of the humeral vein, which often cannot be detected on scaled specimens. Variations were also noted in between the two visible branches of the Sc vein, because an ancestral vein in this location has been hypothesized to constrain wing pattern , and variations were noted at the location where the Rs4 vein terminates because, although this vein does not terminate along the costa in any of the species examined for the present study, it does terminate along the costa in Micropterix  and occasionally in fossil Micropterigidae . To create illustrations, a forewing was photographed while backlit so that both the patterning and venation were visible. This photograph was used as a template for a wing venation/wing patterning illustration created in the vector graphics application Affinity Designer. All intraspecific variation was incorporated into one single illustration per species. For each species, the illustrated wing pattern is that which is most prevalent; each variation is noted by a number and illustrated with a line comprised of red dashes alternating with the color that is present in the variation. Furthermore, supplemental material includes a written description of each pattern variation as well as prevalence data (Additional file 1: Tables S1, S2, S3).
The location of the wing vein 1A + 2A could not be observed in all pinned specimens because of the overlap between the forewing and hindwing, and therefore had to be inferred based on wing slides and previously described venation [40, 61, 62]; however, this vein is of no relevance to the model because it does not reach the costal margin. Similarly, the jugal lobe was often folded in the specimens examined; its outline was inferred based on wing slides and previous descriptions. These and other inferred features are illustrated with dashed lines. In descriptions presented in the Results, the humeral vein is often excluded from statements regarding wing veins that terminate along the costa, because this vein is so often difficult to observe.
We wish to thank George Gibbs (Victoria University of Wellington); Ted Edwards, Marianne Horak, Alan Landford, You Ning Su, and Andreas Zwick (Australian National Insect Collection); David Rowell (Australian National University); and Don Davis, Mignon Davis, Conrad Labandeira, and M Alma Solis (Smithsonian Institution) for discussion and for assistance in collections; Joaquín Baixeras for extensive feedback at various stages of this project; and Jerome Goddard, David Lees, Arnaud Martin, and Sead Sabanadzovic for valuable discussion. We also with to thank the two anonymous reviewers who provided insightful feedback that greatly improved the quality of this manuscript.
The research was supported in part by the USDA National Institute of Food and Agriculture project # MIS-012040 and by the Mather Fund of the Mississippi State University Development Foundation. SRS is supported by the National Science Foundation Graduate Research Fellowship Program under grant # DGE-1125191, Australian National University/National Science Foundation Graduate Research Opportunities Worldwide, National Science Foundation Graduate Research Internship Program, and Sigma Xi Grant-in-Aid of Research # G201503151194219.
SRS and RLB designed the study; SRS examined specimens and wrote the paper, which was then edited and approved by both authors.
The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Newbigin MI. Colour in nature; a study in biology. London: J. Murray; 1898.View ArticleGoogle Scholar
- Darwin C. Order Lepidoptera. In: The descent of man, and selection in relation to sex. 1st ed. New York: D. Appleton and Company; 1871. p. 374–409.View ArticleGoogle Scholar
- Wallace AR. I. On the phenomena of variation and geographical distribution as illustrated by the Papilionidæ of the Malayan Region. Trans Linn Soc London. 1865;25:1–71.View ArticleGoogle Scholar
- Bates HW. XXXII. Contributions to an insect fauna of the Amazon Valley. Lepidoptera: Heliconidæ. Trans Linn Soc London. 1862;23:495–566.View ArticleGoogle Scholar
- Müller F. Über die vortheile der mimicry bei schmetterlingen. Zool Anz. 1878;1:54–5.Google Scholar
- Monteiro A, Tong X, Bear A, Liew SF, Bhardwaj S, Wasik BR, Dinwiddie A, Bastianelli C, Cheong WF, Wenk MR, Cao H, Prudic KL. Differential expression of ecdysone receptor leads to variation in phenotypic plasticity across serial homologs. PLoS Genet. 2015;11:e1005529.View ArticlePubMedPubMed CentralGoogle Scholar
- Sekimural T, Madzvamuse A, Wathen AJ, Maini PK. A model for colour pattern formation in the butterfly wing of Papilio dardanus. Proc Biol Sci. 2000;267:851–9.View ArticleGoogle Scholar
- Wilts BD, IJbema N, Stavenga DG. Pigmentary and photonic coloration mechanisms reveal taxonomic relationships of the Cattlehearts (Lepidoptera: Papilionidae: Parides). BMC Evol Biol. 2014;14:160.View ArticlePubMedPubMed CentralGoogle Scholar
- Finkbeiner SD, Briscoe AD, Reed RD. Warning signals are seductive: relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies. Evolution. 2014;68:3410–20.View ArticlePubMedGoogle Scholar
- Regier JC, Mitter C, Zwick A, Bazinet AL, Cummings MP, Kawahara AY, Sohn J-C, Zwickl DJ, Cho S, Davis DR, Baixeras J, Brown J, Parr C, Weller S, Lees DC, Mitter KT. A large-scale, higher-level, molecular phylogenetic study of the insect order Lepidoptera (moths and butterflies). PLoS One. 2013;8:e58568.View ArticlePubMedPubMed CentralGoogle Scholar
- Regier JC, Mitter C, Kristensen NP, Davis DR, van Nieukerken EJ, Rota J, Simonsen TJ, Mitter KT, Kawahara AY, Yen S-H, Cummings MP, Zwick A. A molecular phylogeny for the oldest (nonditrysian) lineages of extant Lepidoptera, with implications for classification, comparative morphology and life-history evolution. Syst Entomol. 2015;40:671–704.Google Scholar
- Schachat SR, Brown RL. Color pattern on the forewing of Micropterix (Lepidoptera: Micropterigidae): insights into the evolution of wing pattern and wing venation in moths. PLoS One. 2015;10:e0139972.View ArticlePubMedPubMed CentralGoogle Scholar
- Brown RL, Powell JA. Description of a new species of Epiblema (Lepidoptera: Tortricidae: Olethreutinae) from coastal redwood forests in California with an analysis of the forewing pattern. Pan-Pac Entomol. 1991;67:107–14.Google Scholar
- Baixeras J. An overview of genus-level taxonomic problems surrounding Argyroploce Hübner (Lepidoptera: Tortricidae), with description of a new species. Ann Entomol Soc Am. 2002;95:422–31.View ArticleGoogle Scholar
- Zhang W, Shih C, Labandeira CC, Sohn J-C, Davis DR, Santiago-Blay JA, Flint O, Ren D. New fossil Lepidoptera (Insecta: Amphiesmenoptera) from the Middle Jurassic Jiulongshan Formation of Northeastern China. PLoS One. 2013;8:e79500.View ArticlePubMedPubMed CentralGoogle Scholar
- Sukatsheva ID, Vassilenko DV. New taxa of caddisflies (Insecta, Trichoptera) with reduced forewing venation from the Mesozoic of Asia. Paleontol J. 2013;47:77–83.View ArticleGoogle Scholar
- Kukalova-Peck J, Willmann R. Lower Permian “mecopteroid-like” insects from central Europe (Insecta, Endopterygota). Can J Earth Sci. 1990;27:459–68.View ArticleGoogle Scholar
- Minet J, Huang D-Y, Wu H, Nel A. Early Mecopterida and the systematic position of the Microptysmatidae (Insecta: Endopterygota). Ann la Société Entomol Fr. 2010;46:262–70.View ArticleGoogle Scholar
- Comstock J. The Wings of Insects. Ithaca: Comstock Publishing Company; 1918.Google Scholar
- Hashimoto S. A taxonomic study of the family Micropterigidae (Lepidoptera, Micropterigoidea) of Japan, with the phylogenetic relationships among the Northern Hemisphere genera. Bull Kitakyushu Museum Nat Hist Hum Hist (series A, Nat Hist). 2006;4:39–109.Google Scholar
- Lemche H. The primitive colour-pattern on the wings of insects and its relation to the venation. Vidensk meddelelser fra Dansk naturhistorisk Foren i Kjobenhavn. 1935;99:45–64.Google Scholar
- Lemche H. Studien über die Flügelzeichnung der Insekten. I, Hepialina, Micropterygina, Tineoidea, Castnoidea und Zygaenina. Saet af Zool Jahrbücher, Abteilung für Anat und Ontog der Tiere. 1937;63:183–288.Google Scholar
- Nijhout HF. The Development and Evolution of Butterfly Wing Patterns. Washington DC: Smithsonian Institution Press; 1991.Google Scholar
- Süffert F. Zur vergleichende Analyse der Schmetterlingszeichnung. Biol Zent Bl. 1927;47:385–413.Google Scholar
- Schwanwitsch B. On the groundplan of wing-pattern in nymphalids and certain other families of rhopalocerous butterflies. Proc Zool Soc London. 1924;34:509–28.Google Scholar
- Otaki JM. Color pattern analysis of nymphalid butterfly wings: revision of the nymphalid groundplan. Zoolog Sci. 2012;29:568–76.View ArticlePubMedGoogle Scholar
- Nijhout HF. Symmetry systems and compartments in Lepidopteran wings: the evolution of a patterning mechanism. Development. 1994;Supplement:225–33.Google Scholar
- Nijhout HF. 3. Coloration: patterns and morphogenesis. In: Lepidoptera, Moths and Butterflies: Vol 2: Morphology, Physiology, and Development. Hawthorne: Walter de Gruyter; 2003. p. 23–38.Google Scholar
- Reed RD, Gilbert LE. Wing venation and Distal-less expression in Heliconius butterfly wing pattern development. Dev Genes Evol. 2004;214:628–34.View ArticlePubMedGoogle Scholar
- Oliver JC, Robertson KA, Monteiro A. Accommodating natural and sexual selection in butterfly wing pattern evolution. Proc R Soc B. 2009;276:2369–75.View ArticlePubMedPubMed CentralGoogle Scholar
- Mouro LD, Zatoń M, Fernandes ACS, Waichel BL. Larval cases of caddisfly (Insecta: Trichoptera) affinity in Early Permian marine environments of Gondwana. Sci Rep. 2016;6:19215.View ArticlePubMedPubMed CentralGoogle Scholar
- Sohn J-C, Labandeira CC, Davis DR. The fossil record and taphonomy of butterflies and moths (Insecta, Lepidoptera): implications for evolutionary diversity and divergence-time estimates. BMC Evol Biol. 2015;15:12.View ArticlePubMedPubMed CentralGoogle Scholar
- Sohn J-C, Labandeira CC, Davis DR, Mitter C. An annotated catalog of fossil and subfossil Lepidoptera (Insecta: Holometabola) of the world. Zootaxa. 2012;3286:1–132.Google Scholar
- Whalley P. The systematics and palaeogeography of the Lower Jurassic insects of Dorset, England. Bull Br Museum. 1986;39:107–89.Google Scholar
- Grimaldi D, Engel MS. Evolution of the Insects. New York: Cambridge University Press; 2005.Google Scholar
- Ansorge J. Revision of the “Trichoptera” described by Geinitz and Handlirsch from the Lower Toarcian of Dobbertin (Germany) based on new material. Proc 10th Int Symp Trichoptera - Nov Suppl Entomol. 2002;15:55–74.Google Scholar
- Liu Y, Zhang W, Yao Y, Ren D. A new fossil of Necrotauliidae (Insecta: Trichoptera) from the Jiulongshan formation of China and its taxonomic significance. PLoS One. 2014;9:e114968.View ArticlePubMedPubMed CentralGoogle Scholar
- Common I. A new family of Dacnonypha (Lepidoptera) based on three new species from southern Australia, with notes on the Agathiphagidae. J Aust Entomol Soc. 1973;12:11–23.View ArticleGoogle Scholar
- Gibbs GW, Lees DC. New Caledonia as an evolutionary cradle: a re-appraisal of the jaw-moth genus Sabatinca (Lepidoptera: Micropterigidae) and its significance for assessing the antiquity of the island’s fauna. In: Guilbert E, Robillard T, Jourdan H, Grandcolas P, editors. Zoologia Neocaledonica 8. Biodiversity studies in New Caledonia. Paris: Muséum national d’Histoire naturelle; 2014. p. 239–66.Google Scholar
- Davis DR, Landry JF. A review of the North American genus Epimartyria (Lepidoptera, Micropterigidae) with a discussion of the larval plastron. Zookeys. 2012;183:37–83.View ArticlePubMedGoogle Scholar
- Simonsen TJ. The wing vestiture of the non‐ditrysian Lepidoptera (Insecta). Comparative morphology and phylogenetic implications. Acta Zool. 2001;298:275–98.Google Scholar
- Gibbs GW. Micropterigidae (Insecta: Lepidoptera). Fauna New Zeal. 2014;72:1–81.Google Scholar
- Lees DC, Rougerie R, Christof ZL, Kristensen NP. DNA mini-barcodes in taxonomic assignment: a morphologically unique new homoneurous moth clade from the Indian Himalayas described in Micropterix (Lepidoptera, Micropterigidae). Zool Scr. 2010;39:642–61.View ArticleGoogle Scholar
- Zeller-Lukashort HC, Kurz ME, Lees DC, Kurz MA. A review of Micropterix Hübner, 1825 from northern and central Europe (Micropterigidae). Nota Lepidopterol. 2007;30:235–98.Google Scholar
- Wootton RJ. Function, homology and terminology in insect wings. Syst Entomol. 1979;4:81–93.View ArticleGoogle Scholar
- Martin A, Reed RD. Wnt signaling underlies evolution and development of the butterfly wing pattern symmetry systems. Dev Biol. 2014;395:367–78.View ArticlePubMedGoogle Scholar
- Eimer G, Fickert C. Orthogenesis Der Schmetterlinge: Ein Beweis Bestimmt Gerichteter Entwicklung Und Ohnmacht Der Natürlichen Zuchtwahl Bei Der Artbildung. Leipzig: Verlag von Wilhelm Engelmann; 1897.Google Scholar
- Eimer T. Die Artbildung Und Verwandtschaft Bei Den Schmetterlingen. Jena: G. Fischer; 1889.View ArticleGoogle Scholar
- von Linden M. Le dessin des ailes des lépidoptères: recherches sur son évolution dans l’ontogenèse et la phylogenèse des espèces son origine et sa valeur systématique. Ann des Sci Nat Zool. 1902;8:1–196.Google Scholar
- Braun AF. Evolution of the color pattern in the microlepidopterous genus Lithocolletis. J Acad Nat Sci Philadelphia. 1914;16:103–71.Google Scholar
- Eyer JR. The comparative morphology of the male genitalia of the primitive Lepidoptera. Ann Entomol Soc Am. 1924;17:275–342.View ArticleGoogle Scholar
- Ford EB. Problems of heredity in the Lepidoptera. Biol Rev. 1937;12:461–501.View ArticleGoogle Scholar
- Kühn A, Henke K. Eine Mutation der Augenfarbe und der Entwicklungsgeschwindigkeit bei der Mehlmotte Ephestia kühniella Z. Wilhelm Roux’Archiv für Entwicklungsmechanik der Org. 1930;122:204–12.View ArticleGoogle Scholar
- Kühn A, Henke K. Genetische und Entwicklungsphysiologische Untersuchungen an der Mehlmotte Ephestia kühniella Zeller (I-VII). Abhandlungen der Gesellschaft der Wissenschaften Göttingen, Math Klasse. 1936;15:1–2.Google Scholar
- Heikkilä M, Mutanen M, Wahlberg N, Sihvonen P, Kaila L. Elusive ditrysian phylogeny: an account of combining systematized morphology with molecular data (Lepidoptera). BMC Evol Biol. 2015;15:260.View ArticlePubMedPubMed CentralGoogle Scholar
- Kristensen NP. Resolving the basal phylogeny of Lepidoptera: morphological evidence. Entomol Abhandlungen. 2003;61:167–9.Google Scholar
- Oliver JC, Tong X, Gall LF, Piel WH, Monteiro A. A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression. PLoS Genet. 2012;8:e1002893.View ArticlePubMedPubMed CentralGoogle Scholar
- Schachat SR, Oliver JC, Monteiro A. Nymphalid eyespots are co-opted to novel wing locations following a similar pattern in independent lineages. BMC Evol Biol. 2015;15:20.View ArticlePubMedPubMed CentralGoogle Scholar
- Martin A, Reed RD. wingless and aristaless2 define a developmental ground plan for moth and butterfly wing pattern evolution. Mol Biol Evol. 2010;27:2864–78.View ArticlePubMedGoogle Scholar
- Werner T, Koshikawa S, Williams TM, Carroll SB. Generation of a novel wing colour pattern by the Wingless morphogen. Nature. 2010;464:1143–8.View ArticlePubMedGoogle Scholar
- Gibbs GW, Kristensen NP. Agrionympha, the long-known South African jaw moths: a revision with descriptions of new species (Lepidoptera, Micropterigidae). Zootaxa. 2011;2764: 1–21.Google Scholar
- Gibbs GW. Micropterigidae (Lepidoptera) of the Southwestern Pacific: a revision with the establishment of five new genera from Australia. New Caledonia and New Zealand: Zootaxa. 2010;2520:1-48.Google Scholar
- Kurz MA. On the systematic position of Electrocrania Kusnezov, 1941 with the description of a new species from Baltic amber (Lepidoptera: Micropterigidae). Zootaxa. 2015;4044:446–50.View ArticlePubMedGoogle Scholar