Prospects of evodevo for linking pattern and process in the evolution of morphospace

paul m. brakefield

Evolutionary developmental biology or evo-devo will make crucial contributions over the coming years to exploring the occupancy of mor-phospace. Why do species show the patterns of diversity and disparity they do, and to what extent do such patterns reflect the ways in which phenotypic variation is generated as well as the processes of natural selection? Evo-devo in appropriate study systems is providing the means to explore fully how phenotypic variation is generated by the processes intrinsic to individuals, especially those of development. Substantial progress will be made in understanding the occupancy of morphospace if the results of this type of evo-devo can then be combined with analyses of how this same variation is influenced by natural selection and other extrinsic processes to result in the patterns of evolution. Use can also be made here of recent advances in developing appropriate null models for testing adaptive versus neutral or random-walk explanations of evolution (Pie and Weitz 2005).

In combination, this type of broad evo-devo and evolutionary biology can begin to unravel how evolvability, the capacity to evolve at the genetical and developmental levels, contributes to shaping the evolution of patterns of diversity and disparity in phenotypic space (Brake-field 2006). We will then be able to examine the extent to which such phenomena as genetic channelling, developmental bias and developmental drive are reflected in patterns of evolution, whether involving change or stasis (e.g. Maynard Smith et al. 1985, Schluter 1996, Wagner and Altenberg 1996, Arthur 2001, Blows and Hoffman 2005).

Evolving Pathways: Key Themes in Evolutionary Developmental Biology, ed. Alessandro Minelli and Giuseppe Fusco. Published by Cambridge University Press. # Cambridge University Press 2008.

Developmental biology has flourished as the application of new molecular and genetical tools in several model organisms has opened up the mechanisms of development. Differences in embryonic development have been explored across such highly divergent organisms as flies, nematode worms, fish, frogs, chickens and mice. Specific genes and genetic 'toolkit' pathways central to development have been identified through the study of the consequences of major mutations obtained from mutant screens in the model organisms. It is becoming clear that much of the evolution of morphological diversity is about teaching old genes new tricks, and that this frequently does not involve changes in the encoding sequences themselves but rather evolutionary tinkering in their complex regulatory apparatus (Carroll 2005).

Development is central to evolution because the processes of development map morphologies on to genotypes, and differences in development among genotypes generate the variation in phenotype on which selection can act. Developmental biology has been slow to expand upon the work with highly divergent model organisms to examine more subtle differences in form such as are found within a single lineage and which provide the developmental basis of variation in natural populations. However, through the application of evo-devo, variation in form can now be traced on to genetic variation via developmental mechanisms and the processes of pattern formation. A full understanding of the roles of genetic variation in morphological evolution will require an effective integration of the mechanisms of development with studies of evolution. This will need to be done both for variation in form among species with known phylogenetic relationships, and for the variability within the populations of single species. The extent to which this latter level of variation within populations will inform us about the fixed differences that characterise related species is at present unclear but will only be resolved as both levels are examined within particular lineages. This will need to be achieved for many morphologies that are relevant in an ecological arena, such as interactions with potential mating partners or with predators (Brakefield et al. 2003, Brakefield and French 2006).

There is an undoubted power in studying natural genetic variation in developmental processes in a lineage that includes one of the model organisms of developmental biology. For example, work on butterfly wings is successfully building on developmental insights about wing development from Drosophila whilst at the same time taking advantage of the exciting opportunities presented by the well-known ecology in this group (Beldade and Brakefield 2002, McMillan et al. 2002,

Joron et al. 2006). Indeed, one vigorous aspect of evo-devo is that it is rapidly expanding to include new, emerging model organisms which lend themselves to studies both in the laboratory and in the wild. Studies on Heliconius butterflies, dung beetles, stalk-eyed flies, fruit flies, nematode worms, centipedes, and stickleback, cichlid and danio fish all spring to mind (for references see Brakefield et al. 2003, Brake-field and French 2006). This body of work is also ranging widely over differing morphologies from body plans and larval forms through to skeletal morphology, patterns of pigmentation and bristles, and structures such as horns, spines, segments, eyes and so on. Developmental plasticity is becoming better represented, for example in research with butterfly wing patterns, beetle horns, Daphnia helmets and aphid wings. Eventually, this wide net across the animal kingdom and different morphologies will capture many of the general properties of how the genetic variation that underlies developmental change influences patterns in the evolution of animal forms. Such generalisations will become easier as the comparative approaches to variation in form and function for specific morphologies become more integrated with the detailed studies of variation in genetical and developmental mechanisms in the laboratory. One case study that illustrates an integrative approach to linking the evolution of developmental mechanisms with understanding the role of development in evolution is work on wing eyespots and other traits in Bicyclus butterflies.

eyespots matter

Butterfly wings are decorated by mosaics made up of scale cells in patterns resembling the overlapping tiles of a roof. An eyespot is one example of a wing pattern element, and is made up of concentric rings of modified epithelial cells. The scale cells in the eyespot rings syn-thesise different colour pigments in the course of their development. Each eyespot in Bicyclus butterflies usually has a central white pupil surrounded by a middle black ring and an outer gold ring. Eyespots in Bicyclus and other butterflies and moths (together, the Lepidoptera) are known to function both in interactions with predators (Stevens 2005, Brakefield and Frankino 2007) and during courtship and mate choice (Breuker and Brakefield 2002, Robertson and Monteiro 2005). Thus both natural selection and sexual selection are relevant to understanding functional differences in eyespot patterns among species.

Field experiments with Bicyclus butterflies in Malawi have taken advantage of the phenomenon of seasonal polyphenism to show that eyespot patterns can strongly influence adult survival (Brakefield and Frankino 2007). Species of Bicyclus (Nymphalidae: Satyrinae) in regions of Africa with wet-dry seasonal cycles have evolved developmental plasticity. They exhibit seasonal forms differing dramatically in colour pattern on their ventral wing surfaces, especially with respect to the expression of the marginal eyespots (Figure 4.1). The ventral wings are exposed to predators when the butterflies are at rest on the forest floor or feeding on fallen fruit with their wings closed above the body. In each polyphenic species, both of Bicyclus and many other satyrine genera, the dry-season form (DSF) is a more or less uniformly brown insect whereas butterflies of the wet-season form (WSF) have a series of marginal eyespots and a pale medial band across both wings (Brake-field and Larsen 1984, Windig et al. 1994). The essential idea about the adaptive significance of the developmental plasticity is that natural selection in the dry season favours a comparatively inactive or quiescent life style in which butterflies spend most of their time at rest on brown leaf litter. They rely on background matching and crypsis or camouflage (i.e. looking like dead leaves) to survive the long dry season before they can reproduce at the onset of rains, laying eggs on newly green and growing grasses. In contrast, butterflies of the wet-season form are active, reproduce quickly, and rely on marginal eyespots as active deflection devices against vertebrate predators (Brakefield and Larsen 1984, Lyytinen et al. 2004, Stevens 2005); if an attack is aimed at a 'target' eyespot, a butterfly can escape albeit with the loss of some wing tissue grabbed by the predator.

Cohort analyses using mark-release-recapture experiments were performed with Bicyclus butterflies in Malawi to test this hypothesis (Brakefield and Frankino 2007). Here, the results are summarised for the dry season when a colour pattern made more conspicuous by markings like eyespots is predicted to be disadvantageous. Initial experiments used releases of reared butterflies with phenotypes ranging from extreme DSF with no ventral eyespots through to WSF with very large eyespots (Figure 4.2A). Butterflies were released in a forest environment and recaptured using about 40 fruit-baited traps. Patterns of movement over the traps were similar for the different phenotypes. In the dry season, butterflies of the WSF had a much lower probability of recapture than those of the DSF. However, experiments using releases of bred individuals do not demonstrate that it is the ventral eyespots per se that account for higher mortality of the WSF in the dry season since we know that the seasonal forms differ for a suite of traits including physiology and life history.

0 0

Post a comment