Multiple recent co-options of Optix associated with novel traits in adaptive butterfly wing radiations
© Martin et al.; licensee BioMed Central Ltd. 2014
Received: 28 September 2013
Accepted: 27 November 2013
Published: 5 February 2014
While the ecological factors that drive phenotypic radiations are often well understood, less is known about the generative mechanisms that cause the emergence and subsequent diversification of novel features. Heliconius butterflies display an extraordinary diversity of wing patterns due in part to mimicry and sexual selection. Identifying the genetic drivers of this crucible of evolution is now within reach, as it was recently shown that cis-regulatory variation of the optix transcription factor explains red pattern differences in the adaptive radiations of the Heliconius melpomene and Heliconius erato species groups.
Here, we compare the developmental expression of the Optix protein across a large phylogenetic sample of butterflies and infer that its color patterning role originated at the base of the neotropical passion-vine butterfly clade (Lepidoptera, Nymphalidae, Tribe: Heliconiini), shortly predating multiple Optix-driven wing pattern radiations in the speciose Heliconius and Eueides genera. We also characterize novel Optix and Doublesex expression in the male-specific pheromone wing scales of the basal heliconiines Dryas and Agraulis, thus illustrating that within the Heliconinii lineage, Optix has been evolutionarily redeployed in multiple contexts in association with diverse wing features.
Our findings reveal that the repeated co-option of Optix into various aspects of wing scale specification was associated with multiple evolutionary novelties over a relatively short evolutionary time scale. In particular, the recruitment of Optix expression in colored scale cell precursors was a necessary condition to the explosive diversification of passion-vine butterfly wing patterns. The novel deployment of a gene followed by spatial modulation of its expression in a given cell type could be a common mode of developmental innovation for triggering phenotypic radiations.
Adaptive or phenotypic radiations are defined by ‘the evolution of phenotypic diversity within a rapidly multiplying lineage’[1, 2] and form crucibles of natural variation for the study of distinctness, as illustrated by Darwin’s work on Galapagos finches. Ecological arguments involving external (biotic or abiotic) factors are traditionally invoked to explain why phenotypic disparity is maintained over time, but they fail to explain the variation-generating mechanisms that allow these rapid bouts of evolution to occur. Recently, a handful of studies focusing on the intrinsic causes of adaptive radiations showed that diversification could follow relatively simple developmental innovations[4–9]. What principles underlie the emergence of new features, and how do these features further diversify[10, 11]? A meaningful answer to this question may come from comparisons between many organisms, and adaptive radiations assist us in this task by providing a replicated and diverse template of phenotypic variation. Heliconius butterflies are perhaps one of the best studied examples of a phenotypic radiation[13–15]. The genus comprises 40 species distributed across the Neotropics and is characterized by a variegated mosaic of wing patterns that vary both among and within species[13, 16]. Wing patterns commonly function in nature as aposematic traits (that is, as signals displayed to warn potential predators of danger), and butterflies such as Heliconius erato and Heliconius melpomene are a well-known example of this phenomenon. Both species signal their unpalatability by displaying similar wing patterns that are indistinguishable from each other, are endemic to a restricted geographical range, and almost always include red coloration. This Müllerian (that is, reciprocal) mimicry provides a strong adaptive advantage and predators learn to avoid all co-mimics. In fact, most Heliconius species display extensive geographic variation in discrete wing patterns; more than 300 Heliconius regional morphs are recognized by their distinct wing pattern phenotypes and are each locally involved in complex mimicry rings with other co-mimetic butterflies[16, 19, 20].
Many ecological factors explain the diversity of Heliconius butterflies such as their co-evolution with host plants of the Passiflora genus[22, 23] and their participation in dynamic co-mimetic communities[19, 24]. However, these extrinsic factors remain mute regarding the mechanisms that generate wing pattern variation in the first place. Mapping experiments taking advantage of intraspecific variability in the genus have begun to shed light on this question, and have revealed a monogenic (Mendelian) genetic architecture for discrete allelic variation in red patterns[25–27]. In particular, it was found that cis-regulatory evolution of the optix transcription factor is responsible for the presence/absence of red wing patterns in convergent forms of the H. erato and H. melpomene species, as well as in the divergent Heliconius cydno and Heliconius pachinus morphs[28, 29]. Genetic variation at the optix locus explains a large fraction of the diversity of wing patterns in the genus, and was also found to contribute to the convergent evolution of mimetic forms by introgression of optix alleles in related lineages, resulting in a scattered phylogenetic distributions of adaptive patterns[15, 18, 30–32]. Thus, optix incarnates an emblematic example of ‘hotspot of evolution’ where the same gene has repeatedly caused phenotypic variation[28, 33]. Interestingly, some of the variable red patterns controlled by optix are not only involved in predation avoidance, but are also drivers of reproductive isolation by assortative mating[34–36], suggesting that optix allelic variation may directly influence speciation rates.
Despite their ecological significance, little is known about the evolutionary origins of optix-positive red color patterns. Drawing conclusions from morphological analyses alone has been challenging because the wing pattern architecture of Heliconius is divergent relative to the nymphalid ground plan[27, 37, 38] - the system of wing pattern homologies that is otherwise broadly conserved across the family Nymphalidae[39, 40]. Here, we generated a polyclonal antibody directed against the Optix protein and compared its immunoreactivity in the developing wings of Heliconius and other butterflies. We found that the role of Optix in color patterning is relatively recent, making it a synapomorphy of neotropical passion-vine butterflies (tribe: Heliconiini), and that Optix was also associated to the development of novel, sexually dimorphic scale structures in basal heliconiines. In the light of previous work, we conclude that co-option of the Optix transcription factor into the color pattern formation process was a key pre-requisite for the diversification of red wing patterns. The co-option of Optix is thus consistent with a two-step innovation/diversification model, where the evolution of a novel character followed by its spatial modulation generated a wide array of distinct wing patterns.
Polyclonal antibody production
The nucleotide sequence of the H. erato optix gene [GenBank: JN102349.1] was modified using codon degeneracy to artificially lower high GC content without affecting the native amino-acid sequence. The corresponding DNA fragment was generated by gene synthesis (Genewiz,South Plainfield, New Jersey, USA) and cloned into the pQE-30 expression vector (Qiagen, Valencia, California, USA). A 6xHis-Optix fusion protein was expressed in bacterial cultures, extracted in 8 M Urea and purified using Ni2+ affinity column. An insoluble precipitate was recovered upon dialysis and approximately 1 mg was injected in a rat for immunization (5 injections of 200 ug each across 69 days; Covance, Princeton, New Jersey, USA).
Butterfly pupae either originated from individuals collected in southern California, from laboratory colonies maintained at University of Texas - Austin, or from a butterfly farm in Costa Rica [see Additional file1: Table S1]. Whenever possible, the time and day of pupation was monitored. Pupae were then kept at room temperature (23 to 26°C) and dissected on the fourth or fifth day after pupation, a stage at which wings are resistant to shearing while also being permeable to antibodies. Individuals originating from Costa Rica were shipped as untimed pupae and arrived in the laboratory after three days of transit. These pupae were approximately staged by screening their external eye morphology upon receipt. Pupae not presenting mature ommatidial structures (that is, those at an earlier stage of development) were immediately dissected. A portion of these then yielded pupal wing tissues at stages that were early enough for antibody permeability [see Additional file1: Table S1]. The immunohistochemical signal gradually decreases as pupal development proceeds to a point where scale cells begin to mature, the wing epithelia become an opaque white, and the forewings easily detach from the cuticle upon dissection. For all species, dissections performed before this stage resulted in reproducible immunodetection of Optix.
Tissue preparation and immunohistochemistry
Pupae were cold-anesthetized and dissected in PBS. Pupal forewings were incubated in fixative (PBS, ethylene glycol 5 mM tetraacetic acid, 0.01% Triton X-100, 1.85% formaldehyde) for 30 min at room temperature while still attached to their cuticle. Similarly, and in order to maintain flat wing tissues, hindwings were kept attached to their pupal case and fixed for at least 5 min as such, detached by dissection, and then the remainder of the 30 min fixation was completed on free-floating wings. Fixed wings were washed five times with PBST (PBS, 0.5% Triton X-100) and stored at 4°C for up to two months. Wings were cleaned from remnants of peripodial membrane with fine forceps and incubated in blocking buffer for 2 hrs (PBS, 0.5% Triton X-100, 5% Normal Goat Serum; at room temperature), incubated overnight at 4°C with anti-Optix polyclonal rat serum (dilution 1:3000), washed six times with PBST, incubated for 2 hrs at room temperature with an anti-rat IgG Alexa555 (Cell Signaling Technology, Danvers, Massachusetts, USA; 1:2000 dilution), and washed extensively in PBST. Nuclear counterstaining was performed with DAPI, and the wings were mounted in glycerol (PBS, 60% glycerol, 2 mM ethylenediaminetetraacetic acid). F-actin counterstaining was performed using phalloidin conjugated to green fluorescent Oregon Green 488 dye (Life Technologies, Carlsbad, California, USA; 1:400 dilution). For immunostaining in eyes and optic lobes, whole heads were fixed in 4% paraformaldehyde, sucrose protected, and frozen for sectioning. Horizontal sections of 14-μm thickness were made using a cryostat and used for immunohistofluorescence using a previously described procedure. A rabbit anti-UV opsin primary antibody and an anti-rabbit IgG Alexa488 secondary antibody (Cell Signaling Technology, Danvers, Massachusetts, USA; 1:2000 dilution) were used as a positive control in adult eyes. The anti-Doublesex monoclonal mouse antibody was a kind gift of C. Robinett (Janelia Farms Research Campus), was used at a 1:200 dilution and was detected using an anti-mouse IgG Alexa 488 secondary antibody (Cell Signaling Technology, Danvers, Massachusetts, USA; 1:2000 dilution).
Stained tissues were imaged with a Zeiss Axioplan 2 epifluorescence microscope and with a Zeiss LSM 700 confocal microscope. Tiled images were assembled using either the Photomerge function of Adobe Photoshop CS3 (epifluorescence imaging), or were acquired using the Tiled Scan function in the Zeiss ZEN software (confocal imaging). Images were submitted to a linear contrast adjustment to eliminate background illumination.
Other methods are described in the Additional file1: Methods section of this manuscript.
Specific detection of the Optix protein during wing development
Optix was detected during pupal wing development in discrete expression domains that were not associated with color scales. As previously noted, Optix marks the large nuclei of cells that differentiate into spear-shaped acute scales (Figure 1d-e) thought to be involved in wing coupling by frictional effect. Optix was also detected in an anterior domain of small interstitial cells that run along the wing blade of the forewing (Figure 1f-i). In terms of color patterns, Optix was associated with presumptive red scales, including in a small ventral red bar at the base of the forewing costa (Figure 1f-h). We confirmed presumptive color scale correspondence with cellular resolution and in a dorsal-ventral specific-manner. For instance, the red median forewing band of H. erato petiverana differs on its proximal boundary by up to six scale rows between the ventral and dorsal sides. This difference is reflected by corresponding shifts of Optix immunolocalization (Figure 1j-m). These observations provide further verification at the protein level that optix is a selector gene switching on red scale color phenotypes[29, 44].
Conserved color pattern-independent roles of Optix across nymphalid butterflies
Optix reveals homology of red wing patterns among passion-vine butterflies
We replicated the previous observation that Optix expression is associated with the development of red scale patches in Heliconius (Figure 2a), and is in large part responsible for convergent evolution of the Central American H. erato petiverana and H. melpomene rosina co-mimics[29, 45]. To further assess wing pattern homologies across the genus Heliconius we examined the association of Optix with red coloration to additional species and morphs (Figure 2; [see Additional file1: Figure S2]), including Heliconius atthis, which has remarkably divergent red patterns on the hindwing. One notable species we examined, Heliconius doris, is characterized by polymorphic populations where ventral hindwings either display a conspicuous red ray pattern or a more narrow blue or green pattern - discrete variation that is observed within single broods. This variability was present in the stock we assessed (78% red versus 22% non-red individuals; N = 33 emerged butterflies), and was paralleled by Optix immunodetection in a large and rayed ventral patch in 70% (N = 10) of assessed individuals (Figure 2b). Preliminary observations suggest a Mendelian mode of inheritance of H. doris wing patterns, and our result suggests that allelic variation in optix or its upstream regulators is a candidate mechanism for this case of morphological polymorphism.
Optix was consistently detected (with one exception, see below for discussion of Heliconius hecale fornarina) in what we term the ‘proximal complex’, consisting of the red costal forewing bars and of basal hindwing red spots, both situated on ventral wing surfaces (Figures 1j-m and2c). It is unclear whether such small color elements always have an adaptive function in mimicry, but the clear homology between this set of Optix-positive ventral patterns highlights a conserved theme of an otherwise multifarious array of Heliconius wing patterns. This character has deeper roots in the phylogeny, as we positively identified a homologue of the proximal complex in Dryas iulia, which shows Optix-positive scale precursors that mark ventral patches of salmon pink scales. The basal position of D. iulia in the Heliconiini clade [see Additional file1: Figure S4] implies that a color patterning role of Optix preceded the Heliconius radiations, consistent with the observation that many species of the Heliconiini clade harbor unambiguous positional homologs of the proximal complex [see Additional file1: Figure S5]. Similar patterns are not found in heliconiine outgroup lineages, suggesting that the Optix-positive proximal complex is a synapomorphy of the Heliconiini clade of passion-vine butterflies [see Additional file1: Figure S5].
Optix is spatially regulated by the N locus
Optix pinpoints regulatory differences between mimetic orange and red patterns
The hindwings of the butterfly H. hecale fornarina show a claw-shaped ventral pattern that is reminiscent of a similar pattern observed in Heliconius cydno galanthus. Both butterflies co-occur in a large distribution range that spans southern Mexico, Guatemala, and El Salvador, but differ by the yellow versus white color of their forewing bands. However, spectrometer reflectance measurements performed on the H. cydno galanthus and H. hecale fornarina red hindwing patterns [see Additional file1: Figure S6] are almost identical and suggest that natural predators are unable to discriminate between these signals. We previously found that the orange-brown claw pattern of H. cydno expresses optix, and thus wanted to determine whether the H. hecale fornarina pattern would reveal a similar expression pattern. Unexpectedly, we found that Optix was neither expressed in the hindwing claw-shaped pattern nor in the short costal forewing bar (Figure 2c). This negative result indicates that H. hecale fornarina orange/brown color patterning may follow a divergent process. For example, Optix expression could occur at later developmental stages that could not be assayed by our immunostainings. Whatever the explanation, the color patterning role of Optix in silvaniforms - the tiger-like butterflies similar to H. hecale - remains to be determined.
Optix marks presumptive male-specific wing scales in basal Heliconiini
To gain further insights into the development of sexual dimorphism in the wing veins of these butterflies, we sought to test the expression of Doublesex, a transcription factor that has been proposed as a master regulator of sex-specific gene expression and development. An antibody targeting the Drosophila Doublesex DNA-binding domain was recently developed using a conserved antigen. We hypothesized that this antibody would be likely to cross-react with a butterfly Doublesex orthologue, as a BLASTP analysis using the antigenic peptide sequence as a query resulted a single hit with 52 out of 59 conserved residues (88% conservation) against the Heliconius melpomene annotated protein set. Remarkably, immunodetection of Doublesex in Agraulis developing pupal wings specifically marked the dorsal epithelium of the dimorphic veins that include the Optix-positive scale cell precursors (Figure 4c). Only male individuals showed a positive signal among assessed individuals (N = 6, 3 males, 3 females), and all the male veins that are devoid of striated structures - that is, the forewing 1A and all the hindwing veins[50, 51] - showed no Doublesex signal, revealing a tight association of Doublesex expression with sexually dimorphic structures in this system. This result suggests that Doublesex activates the development of the male-specific wing scales via its sex-limited expression, and we speculate that Doublesex could be a transcriptional co-regulator of optix in basal heliconiines.
Optix is expressed in neural progenitors of the optic lobe
The evolutionary origin of red wing patterns in Heliconius is unclear, as these elements seem divergent from the common pattern scheme shared by other butterflies. Here, we clarify this issue by (a) arguing that Optix-positive patterns are a relatively recent novelty that seemingly appeared by co-option of Optix expression in color scale cell precursors, and (b) disentangling different genetic modes of pattern diversification that followed the original co-option event.
Optix color patterns are an evolutionary novelty of passion-vine butterflies
In parallel with its recently evolved color patterning role, Optix also acquired a novel role in the specification of male-specific striated scale structures on the forewing veins of Agraulis butterflies as well as in the basal genus Dryas, suggesting a co-option event prior to the Heliconiini radiation (Figure 6). This implies that Optix has been repeatedly recruited in the specification of derived scale identities, highlighting a possible propensity of the optix gene to be recruited during the evolution of specialized scale types.
Four modes of red pattern diversification in Heliconius
cis-regulatory evolution of optix has played a predominant role in the tinkering of novel red patterns. At least eight optix alleles with distinct pattern-switching effects have been identified by genetic mapping: four alleles in the H. erato/H. himera clade , two alleles in H. melpomene , and two alleles in the H. cydno/Heliconius pachinus sister species . It is proposed that this allelic diversity results from the cumulative effect of many tightly linked cis-regulatory sequence variations organized in complex haplotypes and possibly compartmentalized into several pattern-specific cis-regulatory modules . Following the observation that the genetic basis of phenotypic variation is highly repeatable , and that optix regulation maps to a large adjacent intergenic region that could reflect a potential for complex cis-regulatory structure, we extrapolate that direct cis-regulatory evolution of optix may extend to many cases of red pattern heterotopy (spatial shifts) in Heliconius.
While the optix locus tends to explain presence/absence polymorphism of a given pattern element (for example, the forewing band), pattern shape variation can sometimes be explained by epistatic effects with unlinked loci. Several examples have been characterized at various levels. For instance, the early expression of WntA during larval development determines the shape of the red forewing band [27, 64]. We also show here that N spatially regulates Optix pattern shapes in H. melpomene.
Adaptive optix alleles have been shown to introgress across geographic barriers and to create taxonomic mosaics of pattern diversity, where a given pattern of single origin is scattered across the lineage phylogeny . More surprisingly, lateral transfer by hybridization of wing patterns can occur beyond the species boundary . Directly quoting the original report by Gilbert (2003), virtually all departures from the common pattern themes within the cydno clade (for example, H. heurippa, H. timareta, H. pachinus, H. cydno weymeri form gustavi) can be explained by introgression of toolbox elements from H. melpomene. Optix appears to be a core component of this toolbox, and recent genetic data has since confirmed that cross-species introgressions of optix alleles drive multiple examples of mimetic convergence in the ‘melpomene-cydno-silvaniform’ clade [15, 30, 32, 65]. Introgressions do not directly cause the evolution of novel patterning alleles, but propagate adaptive variants across gene pools, and hybrids can display effects of novelty due to epistatic effects between wing pattern loci, as seen in H. heurippa [47, 65]. Introgressions may be a major but previously unsuspected cause of phenotypic disparity across the animal kingdom, and Heliconius optix alleles emerge as a model system of choice to study this phenomenon .
In addition to the effects of loci that act upstream of optix and affect its localization, modifier loci acting downstream of optix may modulate its color output. A likely example occurs in H. melpomene plesseni, where an unidentified mechanism converts optix-positive scales into a highly-UV reflective scale field of white appearance [29, 48]. This epistatic factor of plesseni origin is visible in an artificial ‘Mixed white’ hybrid population, where an unbroken forewing patch of white and red scales expresses optix (Figure 3e).
In summary, 1) cis-regulatory evolution of optix and epistatic interactions with upstream trans-regulatory factors affect the localization and shape of red patterns; 2) introgressions of optix variants maximize the phylogenetic distribution of pre-existing patterns, sometimes resulting in novel, hybrid patterns due to epistatic effects; and 3) unidentified modifier genes can modulate the color output of Optix-positive scale cell precursors. Similar principles may apply to Optix-independent patterns.
Multiple lines of evidence suggest that the regulatory evolution of the optix locus drives morphological radiations in the wings of H. melpomene and H. erato[15, 18, 30, 45]. Regulatory evolution of this locus may also have a direct influence on species richness itself due to assortative mating between butterflies displaying identical red wing patterns[35, 36]. In the light of the present data, we infer that the evolution of Optix color patterning roles sparked the diversification of red wing patterns within the Heliconiini tribe, notably among the spectacular mimetic radiations observed in the genera Heliconius and Eueides. Multiple recruitments of Optix expression into the differentiation of derived wing scales - the red color scale cells, as well as the male-specific vein structures of basal heliconiines - provide compelling examples of developmental innovation, and the genetic co-option event associated to coloration was followed by a rapid radiation in wing patterns. By opening paths to unexplored valleys of the morphospace, gene co-option events may be a general mechanism explaining sudden bursts of phenotypic change.
We are grateful to Angela Kaczmarczyk for helping with recombinant protein purification, Carmen Robinett for sharing the anti-Doublesex antibody, and Theresa Freiburger for butterfly husbandry at UT Austin. Thomas Schilling provided continuous support for this research and we also thank the members of his laboratory for technical assistance and fruitful discussions. This work was supported by the National Science Foundation grant IOS-1052541 to RDR.
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