Evolution of the butterfly eyespot

The evolution of scale-covered lepidopteran wings provided a new landscape for displaying a striking variety of colors and shapes across the flat wing surface. These color patterns function to warn and confuse predators. For example, a flashing eyespot on a moving butterfly wing can startle a potential predator or redirect its attack away from the butterfly's body. Butterfly eyespots, which are pattern elements composed of concentric rings of colored scales (Fig. 6.4), probably have a single evolutionary origin. Eyespot sizes and colors differ not only between butterfly species, but also between the forewings and hindwings of one animal, and even between the dorsal and ventral surfaces of a single wing. Despite the variation in the color, shape, number, and size of butterfly eyespots, the common features of eyespot development reveal key steps in the evolution of this novel pattern element— specifically, the co-option of genes and regulatory circuits for new patterning roles.

Eyespot development is controlled by a discrete organizer called the "focus," a small group of epithelial cells at the center of the developing eyespot field. During butterfly pupation, focal cells induce the surrounding rings of scale-building cells to produce different pigments. Specification of the eyespot focus is indicated by the expression of the homeodomain-containing transcription factor Distal-less (Dll). A novel late pattern of Dll expression in focal cells follows an earlier conserved pattern of Dll expression (which is found in other insects as well) along the distal edge of the wing. The late pattern begins with the deployment of Dll in short rays of cells extending inward from the wing edge in each subdivision of the wing, then resolves to stable expression of Dll in circular fields of cells only in the subdivisions in which eyespot foci will form (Fig. 6.4). The continued expression of Dll in focal cells in specific wing subdivisions reflects the distribution of eyespots on adult butterfly wings. The conservation of Dll expression in the developing eyespot foci of different butterfly species suggests that the novel recruitment of Dll expression was an early event in the evolution of eyespots. Variation in eyespot size has been linked to the Dll locus, indicating the importance of this gene for eyespot evolution.

The evolution of butterfly eyespots entailed much more than the recruitment of Dll expression; indeed, an entire regulatory circuit was co-opted as well. The Hh signaling pathway, which has a conserved function in patterning along the A/P compartment boundary of insect wings (see Chapter 3), has evolved a second wing-patterning role during eyespot formation. Expression of genes in the Hh pathway (hedgehog (hh), patched (ptc), and Cubitus inter-ruptus (Ci)) is modulated in unique patterns within or immediately surrounding eyespot foci (Fig. 6.5). These patterns suggest that this signaling pathway participates in the establishment of the eyespot focus. In addition, a known target gene of the Hh pathway at the wing A/P boundary—the late activation of engrailed (en) in some anterior compartment cells—is regulated by Hh signaling in the eyespot. En expression is upregulated within every eyespot

Figure 6.5

Recruitment of the Hh signaling pathway in developing butterfly eyespots

The Hh signaling pathway plays a conserved role in patterning the A/P compartment boundary during insect wing development. In butterfly wings, this pathway is deployed in a novel pattern during the formation of eyespot foci. Co-option of Hh signaling requires changes in the regulation of members of the pathway including the hh and Ci genes (see text for details). Source: Keys DN, Lewis DL, Selegue JE, et al. Science 1999; 283: 532-534.

Figure 6.5

Recruitment of the Hh signaling pathway in developing butterfly eyespots

The Hh signaling pathway plays a conserved role in patterning the A/P compartment boundary during insect wing development. In butterfly wings, this pathway is deployed in a novel pattern during the formation of eyespot foci. Co-option of Hh signaling requires changes in the regulation of members of the pathway including the hh and Ci genes (see text for details). Source: Keys DN, Lewis DL, Selegue JE, et al. Science 1999; 283: 532-534.

focus, even in foci that develop in the anterior compartment of the butterfly wing, where en-is not typically expressed (Fig. 6.5).

The recruitment of the Hh signaling pathway in the eyespot field is novel in two respects. First, the modulation of hh expression in a novel pattern near developing eyespots is a unique feature of hh expression in the butterfly wing. Second, the expression of ptc and Ci in the posterior compartment and of hh in the anterior compartment of butterfly wings deviates from the compartmentally restricted deployment of these genes in the Drosophila wing. In Drosophila, expression of ptc and Ci is restricted to the anterior compartment because en represses the expression of these genes in the posterior compartment. Consequently, en repression of ptc and Ci must be relieved in butterfly wings so that the Hh pathway can be used in the posterior compartment. The combination of modulated hh expression and release of the repression of ptc and Ci allows the Hh pathway to be activated in each developing eyespot field. The novel deployment of hh, ptc, Ci, and en in developing eyespots probably represents a critical subset of the regulatory changes that led to the co-option of a complete signal transduction circuit.

The diversity of color patterns within eyespots followed from regulatory changes in later stages of eyespot development. Early in butterfly pupal development, a signal from cells in the eyespot focus induces the pigmentation pattern in surrounding rings of scale cells. This inductive event is accompanied by rapid and dynamic changes in gene expression within the developing scale cells. Dll and En protein expression patterns arise again during this later stage in eyespot development, along with the regulatory protein Spalt (Sal). The expression patterns of these genes in eyespot scale-forming cells correlate with the future concentric color rings of the adult eyespot. Interestingly, the relative spatial domains of Dll, En, and Sal protein expression differ among species. No clear one-to-one correspondence exists between any of these proteins and a particular color output (such as an association between, for example, Sal and gold pigmentation in all eyespots). The differing relative spatial distributions of these proteins and eyespot color schemes reflect the remarkable evolutionary flexibility of the regulatory system governing eyespot development. It has been proposed that eyespots evolved from simpler spot patterns of uniform color. The expression of Dll, Sal, and En in the centers of eyespots appears to be a feature shared among eyespots and may offer a clue to eyespot origins. Namely, these proteins may have been expressed in simpler, uniform spot patterns. The evolution of multiringed spots may then have evolved the acquisition of signaling activity by cells expressing these genes and the recruitment of genes induced by this new signaling activity. The divergence of eyespot color schemes may have evolved through evolutionary changes in genetic responses downstream of signaling from the focus (Fig. 6.6).

The development and evolution of butterfly eyespots illustrate two recurring themes in the evolution of novel characters. First, conserved regulatory circuits can be recruited for new roles during the development of novel morphologies. This recruitment requires changes in the regulation of at least one gene, and subsequent deployment of other genes in the circuit may result from existing regulatory linkages, such as a signal transduction pathway. In this way, a large suite of genes may be deployed in a novel structure with just a small number of evolutionary regulatory changes. Second, evolutionary changes in target gene regulation can facilitate morphological diversification of a novel character. As regulatory evolution modifies the genetic interactions within a developmental program, new patterns can emerge both within and between species.

Figure 6.6

The evolution of eyespots from simple spots

It is thought that eyespots evolved from simpler spots of uniform color. Dll and En may have been expressed during the development of these primitive spots. As cells within this spot acquired signaling activity, surrounding cells acquired the ability to express different pigmentation genes. Further recruitment of signal-regulated genes led to the evolution of multiringed eyespots. Different responses to focal signaling among species may underlie different eyespot color schemes.

Figure 6.6

The evolution of eyespots from simple spots

It is thought that eyespots evolved from simpler spots of uniform color. Dll and En may have been expressed during the development of these primitive spots. As cells within this spot acquired signaling activity, surrounding cells acquired the ability to express different pigmentation genes. Further recruitment of signal-regulated genes led to the evolution of multiringed eyespots. Different responses to focal signaling among species may underlie different eyespot color schemes.

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