Conserved Developmental Genes Can Lead to _______ Evolution.

Philos Trans R Soc Lond B Biol Sci. 2008 Apr 27; 363(1496): 1549–1556.

Conserved developmental processes and the formation of evolutionary novelties: examples from butterfly wings

Suzanne V Saenko

¹Section of Evolutionary Biology, Institute of Biological science, Leiden Academy, Kaiserstraat 63, 2311 GP Leiden, The netherlands

Vernon French

²Institute of Evolutionary Biological science, University of Edinburgh, Ashworth Labs, EH9 3JT Edinburgh, UK

Paul One thousand Brakefield

¹Section of Evolutionary Biology, Establish of Biology, Leiden University, Kaiserstraat 63, 2311 GP Leiden, Holland

Patrícia Beldade

^aneSection of Evolutionary Biology, Institute of Biology, Leiden University, Kaiserstraat 63, 2311 GP Leiden, The Netherlands

Abstract

The origin and diversification of evolutionary novelties—lineage-specific traits of new adaptive value—is one of the key issues in evolutionary developmental biology. However, comparative analysis of the genetic and developmental bases of such traits can be hard when they take no obvious homologue in model organisms. The finding that the evolution of morphological novelties oftentimes involves the recruitment of pre-existing genes and/or gene networks offers the potential to overcome this claiming. Knowledge about shared developmental processes obtained from all-encompassing studies in model organisms can then be used to understand the origin and diversification of lineage-specific structures. Hither, we illustrate this approach in relation to eyespots on the wings of Bicyclus anynana butterflies. A number of spontaneous mutations isolated in the laboratory affect eyespots, lepidopteran-specific features, and as well processes that are shared by nearly insects. We discuss how eyespot mutants with disturbed embryonic evolution may help elucidate the genetic pathways involved in eyespot formation, and how venation mutants with altered eyespot patterns might shed lite on mechanisms of eyespot evolution.

Keywords: evolutionary novelties, butterfly eyespots, embryonic development, wing venation, Bicyclus anynana mutants

1. Introduction

One of the main objectives of evolutionary developmental biology (evo–devo) is to understand the mechanisms that underlie the generation and diversification of evolutionary novelties (Muller & Newman 2005), lineage-specific structures that permit new functions and open upwards new adaptive zones (Mayr 1960). However, the genetic and developmental analysis of such traits tin can be a claiming when they are not represented in model organisms, and the comparative method, and then successful in evo–devo, is harder to utilize.

(a) Co-option of conserved developmental pathways in the evolution of novelties

Among the different genetic mechanisms that have been proposed to explicate the origin of novelties, the redeployment of pre-existing genes and developmental pathways, often with changes in the regulation of components therein, has received a great deal of attention (reviewed in True & Carroll 2002). For instance, the highly conserved Wnt signalling pathway, involved in diverse developmental processes in vertebrates, has been implicated in the evolution of turtle shells (Kuraku et al. 2005), and the arthropod limb patterning genes Distal-less and aristaless have been redeployed in the development of horns in a number of beetle species (Moczek & Nagy 2005). Studies in butterflies provide some spectacular examples of pathways that are shared across all insects, and extensively studied in the genetic model Drosophila melanogaster, which are co-opted in the development of wing scales. Formation and pigmentation of these lepidopteran-specific structures involve genes known from fruit wing sensory bristle development (Galant et al. 1998) and eye pigmentation (Beldade et al. 2005; Reed & Nagy 2005), respectively. This type of co-option of genetic pathways offers the potential to dissect the formation of lineage-specific traits by using accumulated noesis of genetics and development gathered from work on classical model organisms.

(b) Butterfly eyespots every bit an example of evolutionary novelty

The study of butterfly eyespots, characteristic pattern elements composed of concentric rings of different colours, has started to shed lite on how novel patterns have arisen and diversified in the Lepidoptera. Eyespots probably evolved from primitive, uniformly coloured spots through the recruitment and modification of conserved developmental genes and pathways, acquisition of signalling activeness, and farther diversification of colour schemes under the influence of natural selection (Brunetti et al. 2001; Monteiro et al. 2006). Their ecological significance in predator abstention and sexual selection is well documented (Stevens 2005; Costanzo & Monteiro 2007), as is the spectacular variation in eyespot morphology beyond species. Eyespot development is amenable to detailed characterization ranging from the genetic pathways involved in establishing the pattern, to the molecular and cellular interactions underlying pattern specification and to the biochemical networks involved in pigment product (reviewed in Beldade & Brakefield 2002).

Models of eyespot formation involve the production and diffusion of one or more signalling molecules from a key eyespot organizer, the focus, and the response of the surrounding epithelial cells to the signal(s) in a threshold-like style, culminating in pigment product (Nijhout 1980; Dilao & Sainhas 2004). The organizer properties of the focus are supported by experiments in early on pupae where transplantation of the focal cells into a unlike position on the wing induces formation of an ectopic eyespot (Nijhout 1980; French & Brakefield 1995). The molecular identity of the betoken, withal, is not known, just both Wingless and Decapentaplegic have recently been proposed every bit candidate morphogens (Monteiro et al. 2006). Moreover, despite the fact that a number of genes including Distal-less and members of the Hedgehog signalling pathway have been implicated in eyespot development (Carroll et al. 1994; Brakefield et al. 1996; Keys et al. 1999), nosotros know little nigh the interactions between them (Evans & Marcus 2006) or how they regulate paint synthesis (Koch et al. 2000) or about the extent to which they contribute to phenotypic variation in eyespot morphology (Beldade et al. 2002).

(c) Bicyclus anynana every bit an emerging 'eyespot evo–devo' model

The tropical nymphalid butterfly Bicyclus anynana has been established every bit a laboratory organisation and used to report the reciprocal interactions betwixt evolutionary and developmental processes underlying the formation of, and variation in, butterfly colour patterns (Beldade et al. 2005, 2007). This arrangement allows united states of america to combine knowledge of ecology (often minimal for classical genetic model species) with experimental tractability, all the way through to the study of the molecular underpinnings of variation in eyespot morphology. Moreover, recently adult genomic resources (Beldade et al. 2007) and factor expression manipulation techniques (Marcus et al. 2004; Ramos et al. 2006) can now be applied to analysing the phenotypically divergent mutant stocks and choice lines (Beldade et al. 2005) available in our laboratory. This type of integrated analysis holds much hope for deepening our noesis well-nigh the origin and diversification of the lineage-specific morphologies such as butterfly eyespots.

Here, we written report on analyses of a number of spontaneous mutations isolated in B. anynana which affect both eyespot morphology and some other, more conserved, developmental processes, such as embryogenesis or wing vein development. Assay of these mutants within the context of what is known from model organisms provides an opportunity to dissect the genetic mechanisms involved in eyespot formation and variation. We show how comparative analysis of disturbed embryonic evolution with mutants described in model insects might aid identify genes involved in eyespot evolution and how mutations that affect wing venation can provide insights into the mechanisms of eyespot germination.

2. Embryonic lethal mutations and eyespot development

We currently maintain five stocks, each segregating for an allele that has a dramatic outcome on eyespot morphology in heterozygotes and that is embryonic lethal in homozygous state. The mechanisms of early embryonic evolution are very well studied in the dipteran D. melanogaster and are condign increasingly better understood in the representatives of other insect orders, such as the coleopteran Tribolium castaneum and the hemipteran Oncopeltus fasciatus (reviewed in Liu & Kaufman 2005), the hymenopteran Nasonia vitripennis (e.yard. Pultz et al. 2005; Lynch et al. 2006) and in the lepidopterans Bombyx mori (Nagy 1995) and Manduca sexta (Kraft & Jackle 1994). To the extent that the genetic mechanisms of embryogenesis are conserved across insects (reviewed in Peel et al. 2005; Damen 2007), a comparing of disturbed embryonic evolution in B. anynana eyespot mutants with studies of insect model species may assistance identify signalling pathways and/or specific genes involved in eyespot formation and variation.

(a) Embryonic development in B. anynana

Embryonic development in wild-type B. anynana is similar to that described for other Lepidoptera (Nagy 1995). Nosotros analysed the patterns of expression of several conserved developmental genes in wild-type embryos staged according to the arrangement developed for Yard. sexta (Broadie et al. 1991). In a way like to early embryos of Drosophila and Schistocerca americana (Davis et al. 2005), the DP311 antibody in B. anynana detects patterns that are consistent with the expected expression of the segment polarity gene gooseberry, as well equally the patterns in the head and in the tips of the appendages that may reflect expression of the homeobox genes, Rx and aristaless (figure 1 a,b). Also, resembling their counterparts in Drosophila and a number of lepidopterans (Patel et al. 1989; Panganiban et al. 1994; Zheng et al. 1999), the products of the segment polarity genes wingless and engrailed are detected in a reiterated mode in all embryonic segments (figure 1 c,d), whereas the transcription factors Distal-less and Ultrabithorax/Abdominal-A are detected in the tips of the appendages (figure 1 d) and in the abdominal segments (figure 1 due east), respectively. The conservation of some aspects of embryonic evolution (namely, segment patterning by segment polarity and Hox genes, and limb patterning by Distal-less) equally illustrated by these results suggests that the study of disrupted embryonic development in the pleiotropic B. anynana eyespot mutants could be useful for identifying genes and pathways involved in eyespot formation.

Expression patterns of developmental genes in B. anynana embryos (ventral view in (a–d); lateral view in (e), scale bar 0.1 cm). (a) At 15% developmental time (DT), DP311 antibiotic (Davis et al. 2005) detects the segment polarity protein Gooseberry in each embryonic segment, and probably the homeobox protein Rx in the head (arrow). (b) At 20% DT, the same antibiotic also detects a pattern in the tips of limb primordia (arrow) that is probable to exist Aristaless. (c) At 25% DT, wingless mRNA is detected in a segmentally reiterated fashion. (d) At 30% DT the proteins Engrailed (dark-green; anti-En antibody 4F11, Patel et al. 1989) and Distal-less (scarlet; anti-Dll antibody, Panganiban et al. 1994) are detected in the posterior segment compartments and in the tips of the appendages, respectively. (e) The antibody FP6.87 (Kelsh et al. 1994) detects Ultrabithorax and Abdominal-A in the intestinal segments at 50% DT. Antibody staining was performed according to Patel et al. (1989). In situ hybridization was performed as described in Tautz & Pfeifle (1989), using digoxigenin-labelled riboprobe against a 315 bp fragment of the B. anynana wingless gene (AY218276) and carried out at 55°C for 48 hours. Control reaction with sense-strand probe produced no staining.

(b) Embryonic lethality in homozygous Goldeneye mutants

Ane of the mutations showing lethality in homozygotes, Goldeneye, has been previously described equally a ascendant autosomal allele (Brunetti et al. 2001). It disturbs eyespot colour limerick in the heterozygotes—the scales that typically course the black inner ring of the eyespots in wild-type butterflies are replaced by aureate-coloured scales feature of the outer ring (figure 2 a,b,east,f). The expression blueprint of engrailed in the pupal wings is besides contradistinct and closely corresponds to the changes in the adult scale coloration (figure 2 c,grand; come across also Brunetti et al. 2001).

Wild-type B. anynana (a–d) and Goldeneye mutant (eastward–h). (a,due east) Ventral view of one developed female showing serially repeated eyespots along the margins of the fore and hindwings. (b,f) Enlargement of the posterior eyespot on the ventral surface of the forewing. (c,m) Expression pattern of engrailed in the developing pupal wing corresponds to the distribution of gold-coloured scales in the adult eyespots (staining with anti-En 4F11 equally described in Brunetti et al. (2001); bar=0.02 cm). (d,h) Wild-type embryo subsequently blastokinesis at 50% DT, and embryo homozygous for the Goldeneye allele that failed to undergo blastokinesis (bar=0.ane cm); arrows bespeak to the first thoracic leg.

To investigate the effect of Goldeneye mutation on embryonic development, we analysed segregation of embryonic lethality and adult eyespot morphology in a number of individual families from crosses between Goldeneye individuals. All unhatched embryos from 14 families were dissected and their morphology was compared with that of wild-type embryos. We establish that overall ane quarter of the embryos, presumably those homozygous for the Goldeneye allele, died before hatching and displayed severe abnormalities (465 out of 1901; ratio not significantly heterogeneous amid families, Χ _thirteen ²=x.84). The remaining 75% developed commonly and all hatched larvae from half dozen out of xiv experimental families were reared through to adulthood and scored for eyespot phenotype. Of a total of 386 eclosed adults, 233 had Goldeneye eyespots, consistent with heterozygosity for the mutant allele (2 GE : one WT ratio not significantly heterogeneous amongst families, Χ ₅ ²=i.12). Embryonic defects in Goldeneye homozygotes are detected at the stage of blastokinesis, the characteristic movement of the embryo inside the egg which results in its reversal from a ventral to dorsal flexion. This stage is completed by 50% of developmental time (DT) in the wild-blazon. We found that blastokinesis does non occur in homozygous Goldeneye embryos which subsequently go shorter and thicker and also lack bristles (figure two d,h). Mutant embryos die at approximately 60% DT.

(c) Candidate genes for embryonic lethal mutations

A number of mutations that affect other aspects of embryonic morphology also seem to disturb blastokinesis (east.k. homeotic mutations at the E locus in B. mori; Ueno et al. 1995), but the specific genetic regulation of this procedure is poorly understood. Fifty-fifty though it is unclear how many genes control blastokinesis in butterflies and to what extent the processes of embryonic movements in Lepidoptera and other insects are regulated by similar mechanisms, mutations affecting embryonic movements in insects might provide clues about the genetic basis of the Goldeneye phenotype. Examples include the insect Hox3 orthologue zen which plays a role in the processes of katatrepsis in O. fasciatus (Panfilio et al. 2006) and T. castaneum (Van der Zee et al. 2005), and integrin and laminin genes mutations in which disrupt germ band retraction in Drosophila embryos (Schock & Perrimon 2002). Although described mutant phenotypes for these genes bear witness no morphological resemblance to the Goldeneye embryonic phenotype, these genes might provide a valuable starting indicate for exploring the genetic footing of contradistinct eyespot colour composition in Goldeneye.

We are currently investigating embryonic lethality in four other eyespot mutants, three of which announced to disturb development during the segmented germ band phase which, different blastokinesis, is highly conserved amid arthropods, and the genes and developmental pathways that regulate it have been studied in neat item in model organisms (Galis et al. 2002). Comparison of disturbed segmentation in these eyespot mutants with the phenotypes of segmentation mutants in model systems is likely to reveal many more details about butterfly eyespot germination.

(d) Conservation versus divergence in insect embryonic development

The strategy outlined to a higher place volition exist useful merely to the extent that the genetic mechanisms of embryonic development are conserved across insect orders, enabling straight comparisons to be made with model organisms. Nearly cognition most genetic mechanisms regulating insect embryonic development comes from extensive studies in D. melanogaster (run across Peel et al. 2005). However, a contempo focus on organisms from other insect orders is painting a dissimilar scenario (Damen 2007). While some aspects of embryonic development are indeed remarkably conserved (east.k. the functions of segment polarity and Hox genes), others appear to exist unexpectedly diverged (e.yard. the functions of gap and pair-rule genes; see Pare et al. 2005; Damen 2007). Nevertheless, because straight comparison of disturbed eyespot phenotypes with eyespot mutants in model species is impossible, comparative analysis of mutations with pleiotropic effects is a valuable alternative strategy. If it appears that the specific embryonic phase afflicted by a mutation is one showing bully divergence across species, this strategy volition need to be complemented with a more unbiased, genome-wide search for the genetic factors involved in eyespot formation (east.thou. gene mapping; see Beldade et al. 2002).

3. Wing venation and eyespot germination

Models of wing pattern establishment ofttimes involve an active role of fly veins and the wing margin, but their precise function in colour pattern formation on butterfly wings is not well understood. While description of venation mutants in Papilio and Heliconius butterflies has provided bear witness for the relationship between wing venation and patterns of colourful stripes and bands (Koch & Nijhout 2002; Reed & Gilbert 2004), the role of wing veins in eyespot formation remains untested. Models of eyespot formation take suggested that the wing veins and margin deed as sources of diffusible molecules involved in the decision of the eyespot focal organizer (Nijhout 1991; Evans & Marcus 2006). Wingless and Decapentaplegic accept been proposed equally candidate diffusible signals, based on their role as long-range signalling molecules in Drosophila wing discs (McMillan et al. 2002; Evans & Marcus 2006; Monteiro et al. 2006). A role of wing veins, as well every bit the nature or fifty-fifty the being of the proposed diffusible signals, has not still been shown experimentally.

(a) Parallels between fruit fly and butterfly vein development

The mechanisms of vein patterning in Drosophila have been extensively studied (reviewed in De Celis 2003; Crozatier et al. 2004), and the role of veins in the distribution of melanin precursors in newly eclosed fruit flies has established a functional relationship between venation and pigmentation (True et al. 1999). This noesis volition be crucial for our agreement of vein institution and its role in pattern germination in butterfly wings. Unsurprisingly, positional specification in butterfly wing discs seems to be achieved in a manner very similar to that in the fruit wing. Developing wing discs are divided into anterior–posterior and dorsal–ventral compartments past the expression of the genes engrailed and apterous, respectively, and proximal-distal patterning is presumably regulated by Distal-less and wingless (Carroll et al. 1994). The signalling pathways that are involved in the positioning and differentiation of longitudinal and cross veins in Drosophila (reviewed in Marcus 2001; Crozatier et al. 2004) might also be conserved betwixt the lineages of Diptera and Lepidoptera (De Celis & Diaz-Benjumea 2003). Detailed testing of the functional office of homologues of known Drosophila vein patterning genes during butterfly wing evolution will be crucial to our detailed knowledge of vein establishment and role in butterfly wings.

(b) Mutations affecting venation and eyespot design in B. anynana

Our observation that mutants of B. anynana with disturbed venation also accept aberrations in their eyespot patterns very strongly suggests that eyespot formation depends on normal germination of veins and tracheae. Here we describe three spontaneous mutations with furnishings on vein and eyespot phenotypes (figure 3). In extra veins the improver of a cross vein in a variable position in the distal part of fore- and/or hindwings ofttimes leads to the formation of an extra eyespot (figure 3 a). This presumably happens when the ectopic vein bisects an existing eyespot focus, or because the boosted vein itself acts equally an inducer of eyespot formation. In dissimilarity, the mutations Cyclops (Brakefield et al. 1996) and veinless partially inhibit vein development in the distal role of the fly. In Cyclops adults, loss of several veins typically results in fusion of some eyespots and loss of others (figure 3 b), while in veinless, all veins appear to be at least partially vestigial and eyespots are strongly reduced on the ventral wing surface (effigy iii c), and commonly absent dorsally (figure 3 e). This differential issue on dorsal and ventral eyespots, which is also seen in phenotypic plasticity in response to rearing conditions (Brakefield et al. 1996), might result from differences in timing in the onset of eyespot decision between the two wing surfaces.

Venation mutants of B. anynana (ventral surface of hindwings on (a–c) and dorsal surface of forewings on (d–f)). (a) In this extra veins individual, the additional vein (pointer) accompanies an extra eyespot (compare with wild-type hindwing in figure 2 a). (b) Cyclops mutation causes fractional loss of veins and the fusion of some eyespots and loss of the others. (c) veinless mutation results in vestigial venation and reduction of ventral eyespots. (d) Dorsal surface of a wild-blazon forewing with the two characteristic eyespots, which are absent in veinless adults (e). Grafting of focal tissue from the larger eyespot of a wild-type pupa into a veinless host (cf. French & Brakefield 1995) in the position indicated past the pointer in (e) consistently produced ectopic eyespots in a veinless background (f). Note that faint patterns visible in (eastward,f) are the eyespots present on the ventral wing surface.

(c) Surgical manipulations in the veinless mutant

In relation to the indicate–response model of eyespot formation explained previously, absenteeism of eyespots on the dorsal surface of the forewing in veinless mutants (figure three eastward) can be acquired either by a lack of focal point or by the inability of epidermal cells to reply to that signal. We have investigated these alternatives by transplanting the signalling focus of the large dorsal forewing eyespot from early wild-blazon pupae into the forewing of veinless pupae (figure three d; cf. French & Brakefield 1995). This manipulation consistently resulted in the production of a well-defined ectopic eyespot (figure 3 f) in the otherwise eyespotless wing of veinless collywobbles (figure 3 eastward), showing that the veinless fly epithelium is fully competent to reply to the focal signal in a threshold-dependent way and to synthesize the black and aureate pigments that make upwardly a typical eyespot. Our results advise that the vestigial venation in veinless butterflies is associated with the damage of determination of the eyespot focus and/or production of the focal signal. The molecular mechanisms of this relationship take yet to be explored. Further analysis will include the comparison of the disturbed vein phenotype of B. anynana mutants and well-characterized venation mutants in D. melanogaster to place candidate genes and pathways for mutations in our butterfly.

four. Last remarks

We reported on the analysis of a number of spontaneous mutants in B. anynana butterflies which affect eyespot patterning (a lepidopteran novelty) and other developmental processes that are conserved beyond insects (namely, embryogenesis or fly vein development). Analysis of these mutants in the context of the all-encompassing genetic and developmental noesis bachelor for model systems holds promise for furthering our understanding of the origin and diversification of butterfly eyespots.

(a) Shared developmental processes and evolutionary novelties

Amid the dissimilar genetic mechanisms that have been proposed to account for the origin of novel traits, information technology is the redeployment of existing pathways that is discussed here. The fact that some shared pathways are reutilized to produce novel structures (with more or less modification of the components therein) offers the potential for using the extensive cognition of such pathways coming from model organisms, to understand structures present in other systems. Here, we accept illustrated this arroyo using laboratory mutations in B. anynana with pleiotropic effects on eyespot patterns and either embryonic development or wing venation, both well studied in D. melanogaster. This approach can, in theory, be used to analyse a whole suite of novel traits in whatever insect species provided pleiotropic mutants accept been identified and can be kept in the laboratory.

Wound healing is another example of a fundamental procedure that is likely to be shared by all animals and might have been co-opted in the evolution of eyespots. Damage of wing tissue in early on pupae can lead to the germination of ectopic eyespots (Brakefield & French 1995), probably via the upregulation of expression of characteristic 'eyespot genes' (eastward.one thousand. Distal-less, engrailed and spalt) in scale-building cells effectually the wound site (Monteiro et al. 2006). Detailed analysis of such shared genetic networks in the context of eyespot formation will be invaluable for our understanding of the evolutionary diversification of butterfly eyespots.

(b) Mutations of big event and morphological diversification

A related issue of smashing importance in evo–devo is that of the genetic and developmental mechanisms underlying phenotypic variation. In particular, the extent to which mutants of large effect identified in the laboratory are relevant for natural variation within and across species is a affair of debate (come across Haag & True 2001). While information technology seems unlikely that recessive lethal alleles such equally Goldeneye will contribute to eyespot variation in natural populations (unless there is a potent heterozygote reward), it is possible that the aforementioned loci harbour other alleles, relevant for variation in eyespot patterns. Also, while mutations that eliminate wing veins and lead to rapid wing damage and, consequently, to reduction in flight ability (equally in Cyclops and veinless) are unlikely to be favoured by natural choice, more localized changes in venation or vein additions (equally in actress veins) might be relevant mechanisms for wing pattern evolution. Future work will explore the extent to which loci identified in laboratory eyespot mutants contribute to quantitative variation segregating in natural populations and potentially stock-still across species.

We accept illustrated how studies of B. anynana wing patterns and, in particular, of eyespot mutants, tin shed light on some of the nearly exciting questions in evo–devo. Butterfly eyespots, similar some other evolutionary novelties, have evolved largely via the redeployment of genetic circuitry involved in other, shared, developmental processes. The written report of the latter and the comparing with model insects offer a new approach to studying the origin and diversification of lineage-specific structures.

Acknowledgments

We give thanks Sean Carroll and Nipam Patel for the antibodies they kindly provided, Michael Akam for fruitful discussion and suggestions during the starting time phase of this work, Cerisse Allen for critical comments on this manuscript, Andrew Peel and one anonymous referee for their thoughtful reviews, Arnaud Martin for assist with in situ hybridization of B. anynana embryos and Niels Wurzer and colleagues for assist with rearing butterflies. P.B. is supported by a grant from the Dutch Science Foundation NWO (VENI 863.04.013).

Footnotes

Ane contribution of 17 to a Discussion Meeting Result 'Evolution of the animals: a Linnean tercentenary celebration'.

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Notice of correction

Citations to effigy 2 are now presented in the correct form.

 3 March 2008

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2615821/

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