Bringing Evo Devo to Life

Sean Carroll's book shows how the central black box of development that maps phenotypes onto genotypes is revealing its secrets in many exquisite, and frequently unexpected, ways

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

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 difficult when they have no obvious homologue in model organisms. The finding that the evolution of morphological novelties often involves the recruitment of pre-existing genes and/or gene networks offers the potential to overcome this challenge. Knowledge about shared developmental processes obtained from extensive studies in model organisms can then be used to understand the origin and diversification of lineage-specific structures. Here, 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 also processes that are shared by most insects. We discuss how eyespot mutants with disturbed embryonic development may help elucidate the genetic pathways involved in eyespot formation, and how venation mutants with altered eyespot patterns might shed light on mechanisms of eyespot development

Eyespot Development on Butterfly Wings: The Epidermal Response to Damage

AbstractEyespot colour patterns decorate the wings of many butterfly species. The eyespot is specified in the early pupal epidermis by signals from a central "focus," and it has been suggested that the focus is the source of a diffusible morphogen gradient. We show that ectopic eyespots can be induced in nonfocal positions throughout the distal, but not the proximal, wing epidermis of Bicyclus anynana by mild epidermal damage inflicted at 12-18 hr (into a 6- to 7-day pupal period). Damage may lower, locally and transiently, the threshold for response to morphogen. Here, we have tested two predictions of the gradient model. As predicted, mild damage close to the focus (parafocal) locally extends the eyespot, making it markedly asymmetrical, even after early operations (1 or 6 hr), when remote epidermis is nonresponsive. Early parafocal operations also have an unexpected result, however, reducing the extent of the eyespot in other directions, perhaps through a long-range "wound effect" on the signaling activity of the focal cells. The model also correctly predicts that increasing the severity of a nonfocal operation will prolong the transient damage and hence give ectopic eyespots after early (1- or 6-hr) operations. We do not, however, find the expected size increase in ectopics induced by the later (12 or 18 hr) severe damage. Similarly, we demonstrate the predicted effect of early (1 or 6 hr) mild damage in increasing the response to a subsequent (18 hr) operation at the same position. The gradient model is therefore supported by most aspects of eyespot induction in response to epidermal damage

Identification and Biosynthesis of Novel Male Specific Esters in the Wings of the Tropical Butterfly, Bicyclus martius sanaos

Representatives of the highly speciose tropical butterfly genus Bicyclus (Lepidoptera: Nymphalidae) are characterized by morphological differences in the male androconia, a set of scales and hair pencils located on the surface of the wings. These androconia are assumed to be associated with the release of courtship pheromones. In the present study, we report the identification and biosynthetic pathways of several novel esters from the wings of male B. martius sanaos. We found that the volatile compounds in this male butterfly were similar to female-produced moth sex pheromones. Components associated with the male wing androconial areas were identified as ethyl, isobutyl and 2-phenylethyl hexadecanoates and (11Z)-11-hexadecenoates, among which the latter are novel natural products. By topical application of deuterium-labelled fatty acid and amino acid precursors, we found these pheromone candidates to be produced in patches located on the forewings of the males. Deuterium labels from hexadecanoic acid were incorporated into (11Z)-11-hexadecenoic acid, providing experimental evidence of a Δ11-desaturase being active in butterflies. This unusual desaturase was found previously to be involved in the biosynthesis of female-produced sex pheromones of moths. In the male butterflies, both hexadecanoic acid and (11Z)-11-hexadecenoic acid were then enzymatically esterified to form the ethyl, isobutyl and 2-phenylethyl esters, incorporating ethanol, isobutanol, and 2-phenylethanol, derived from the corresponding amino acids L-alanine, L-valine, and L-phenylalanine

Seasonal environments drive convergent evolution of a faster pace-of-life in tropical butterflies

New ecological niches that may arise due to climate change can trigger diversification, but their colonisation often requires adaptations in a suite of life-history traits. We test this hypothesis in species-rich Mycalesina butterflies that have undergone parallel radiations in Africa, Asia, and Madagascar. First, our ancestral state reconstruction of habitat preference, using c. 85% of extant species, revealed that early forest-linked lineages began to invade seasonal savannahs during the late Miocene-Pliocene. Second, rearing replicate pairs of forest and savannah species from the African and Malagasy radiation in a common garden experiment, and utilising published data from the Asian radiation, demonstrated that savannah species consistently develop faster, have smaller bodies, higher fecundity with an earlier investment in reproduction, and reduced longevity, compared to forest species across all three radiations. We argue that time-constraints for reproduction favoured the evolution of a faster pace-of-life in savannah species that facilitated their persistence in seasonal habitats.Peer reviewe

Systematics and historical biogeography of the old world butterfly subtribe Mycalesina (Lepidoptera: Nymphalidae: Satyrinae).

BACKGROUND: Butterflies of the subtribe Mycalesina have radiated successfully in almost all habitat types in Africa, Madagascar, the Indian subcontinent, Indo-China and Australasia. Studies aimed at understanding the reasons behind the evolutionary success of this spectacular Old World butterfly radiation have been hampered by the lack of a stable phylogeny for the group. Here, we have reconstructed a robust phylogenetic framework for the subtribe using 10 genes from 195 exemplar taxa. RESULTS: We recovered seven well supported clades within the subtribe corresponding to the five traditional genera (Lohora, Heteropsis, Hallelesis, Bicyclus, Mycalesis), one as recently revised (Mydosama) and one newly revised genus (Culapa). The phylogenetic relationships of these mycalesine genera have been robustly established for the first time. Within the proposed phylogenetic framework, we estimated the crown age of the subtribe to be 40 Million years ago (Mya) and inferred its ultimate origin to be in Asia. Our results reveal both vicariance and dispersal as factors responsible for the current widespread distribution of the group in the Old World tropics. We inferred that the African continent has been colonized at least twice by Asian mycalesines within the last 26 and 23 Mya. In one possible scenario, an Asian ancestor gave rise to Heteropsis on continental Africa, which later dispersed into Madagascar and most likely back colonised Asia. The second colonization of Africa by Asian ancestors resulted in Hallelesis and Bicyclus on continental Africa, the descendants of which did not colonise other regions but rather diversified only in continental Africa. The genera Lohora and Mydosama are derivatives of ancestors from continental Asia. CONCLUSION: Our proposed time-calibrated phylogeny now provides a solid framework within which we can implement mechanistic studies aimed at unravelling the ecological and evolutionary processes that culminated in the spectacular radiation of mycalesines in the Old World tropics

Conserved patterns of integrated developmental plasticity in a group of polyphenic tropical butterflies

Background: Developmental plasticity is thought to have profound macro-evolutionary effects, for example, by increasing the probability of establishment in new environments and subsequent divergence into independently evolving lineages. In contrast to plasticity optimized for individual traits, phenotypic integration, which enables a concerted response of plastic traits to environmental variability, may affect the rate of local adaptation by constraining independent responses of traits to selection. Using a comparative framework, this study explores the evolution of reaction norms for a variety of life history and morphological traits across five related species of mycalesine butterflies from the Old World tropics. Results: Our data indicate that an integrated response of a suite of key traits is shared amongst these species. Interestingly, the traits that make up the functional suite are all known to be regulated by ecdysteroid signalling in Bicyclus anynana, one of the species included in this study, suggesting the same underlying hormonal regulator may be conserved within this group of polyphenic butterflies. We also detect developmental thresholds for the expression of alternative morphs. Conclusions: The phenotypic plasticity of a broad suite of morphological and life history traits is integrated and shared among species from three geographically independent lineages of mycalesine butterflies, despite considerable periods of independent evolution and exposure to disparate environments. At the same time, we have detected examples of evolutionary change where independent traits show different patterns of reaction norms. We argue that the expression of more robust phenotypes may occur by shifting developmental thresholds beyond the boundaries of the typical environmental variation