Wallace Arthur

The emerging conceptual framework of evolutionary developmental biology

Over the last twenty years, there has been rapid growth of a new approach to understanding the evolution of organismic form. This evolutionary developmental biology, or ‘evo-devo’, is focused on the developmental genetic machinery that lies behind embryological phenotypes, which were all that could be studied in the past. Are there any general concepts emerging from this new approach, and if so, how do they impact on the conceptual structure of traditional evolutionary biology? In providing answers to these questions, this review assesses whether evo-devo is merely filling in some missing details, or whether it will cause a large-scale change in our thinking about the evolutionary process.

The Evolutionary Consequences of Interspecific Competition

Publisher Summary This chapter describes the degree to which genetic changes in mixed species populations can be ascribed to natural selection resulting from interspecific competition. The chapter discusses the main postulated patterns of competitively-induced evolution, the relevant theoretical models, the development of a series of criteria, and experimental and observational case-studies on a wide range of species. Several possible evolutionary consequences of competition between species have been proposed, and some of these have been developed in detail by theorists. Many experimental and observational case-studies have been conducted in which evolutionary aspects of interspecific competition have been examined. The relative commonness of different co-evolutionary patterns is uncertain. Future studies ought to become more preoccupied with the heritability of characters, more analytic with regard to the meaning of competitive ability and more determined in their attempts to distinguish interspecific competition from other selective agents than the majority of studies conducted to date.

The niche in competition and evolution

Using the concept of the niche (and multiple niche) this book attempts to synthesise two widely-investigated topics: polymorphism and between-species competition; the authors view being that multiple-niche coexistence and multiple- niche polymorphism together represent a common means of coexistence of competitors. Experimental detail and fieldwork are frequently cited in order to create a common point of reference for both population ecologists and geneticists. Concluding chapters discuss other important principles and hypotheses in evolution which are related to the niche concept.

Developmental drive: an important determinant of the direction of phenotypic evolution.

SUMMARY Over any period of evolutionary time, the prevailing ontogenetic trajectory within a lineage may either recur unchanged from generation to generation (stasis) or alter (developmental reprogramming). A key question about reprogramming is whether it exhibits intrinsic biases in favor of some sorts of change and against others, which may be referred to respectively as “drive” and “constraint.” A simple logical argument suggests that both drive and constraint should be common, and conversely that cases of equiprobable modification in various phenotypic directions should be relatively rare. These proposals, that drive and constraint exist and that they are common, appear to be widely accepted, even among neo‐Darwinians, who are sometimes portrayed as rejecting them. What is more controversial is that developmental drive (and constraint) can have a powerful influence on the direction of evolutionary change. It is argued that such an influence will occur, and indeed may be pervasive.

Early development and segment formation in the centipede, Strigamia maritima (Geophilomorpha).

Summary Geophilomorph centipedes exhibit a number of unique characteristics that make them of particular developmental and evolutionary interest. Segment numbers in geophilomorphs are higher than in any other centipedes, ranging from 27 to 191. They may be constant within a species, presenting in extreme form the “counting” problem in development, or they may vary—a situation that provides us with the opportunity to study naturally occurring variation in segment numbers. All their segments are generated during embryogenesis, a situation unlike that in the more basal centipede orders, which generate only a fraction of their 15 trunk segments in the embryo and develop the rest postembryonically. Here we provide a foundation for further developmental studies of the Geophilomorpha, building on the one study that has been conducted to date, on the coastal species Strigamia maritima. Development begins with the migration of nuclei to the surface of the egg, which then condense to form an embryonic rudiment of more than 20,000 cells, covering an entire hemisphere. During early development, the embryo can be divided into two distinct areas: a large terminal disc of apparently undifferentiated tissue and the germ‐band, which has a clear anteroposterior axis and differentiated segments. The germ‐band forms from the anterior of the terminal disc and extends anteriorly as the disc contracts. New segments are formed at the posterior margin of the germ‐band. Once the process of segmentation ends, the germ‐band folds and sinks into the yolk. We note that the classic description of centipede development, by Heymons more than a century ago, contains a fundamental error in the identification of the axes and hence in the interpretation of early segmentation.

The concept of developmental reprogramming and the quest for an inclusive theory of evolutionary mechanisms

SUMMARY Evolutionary developmental biology has already made a major contribution to our understanding of evolutionary patterns, notably homology. However, while it has the potential to make an equally important contribution to our understanding of evolutionary mechanisms, and indeed to the integration of mechanism and pattern, it has not yet done so. This paper explores how this potential may be realized. In particular, I focus on the limitations of present‐day neo‐Darwinian theory, and indicate how a combination of the neo‐Darwinian and “evo‐devo” approaches provides a more inclusive view of evolutionary mechanisms with greater explanatory power. There is a particular focus on developmental reprogramming, which lies logically between mutation and selection, yet has been neglected in mainstream evolutionary theory. The inclusion of developmental reprogramming in the list of evolutionary mechanisms leads to a view that the direction of evolutionary change is determined by a combination of internal and external factors, rather than being controlled entirely by the environment.

The effect of development on the direction of evolution: toward a twenty‐first century consensus

Summary One of the most important questions in evolutionary biology is: what orients the evolutionary process? That is, what causes evolution to proceed toward certain developmental trajectories, and hence phenotypes, rather than others? In particular, there has been prolonged controversy over whether the direction of evolution is determined solely by external factors or whether the nature of the ontogenetic process, and the ways in which it can be altered by mutations in developmental genes, may also play a major role. Here, I examine this issue, concentrating on the following: the possible evolutionary orienting role of “developmental bias;” the question of whether selection can and/or will break bias; the extent to which bias is already incorporated in quantitative genetic studies; and ways of approaching the possible role of bias in the origin of evolutionary novelties. Finally, I suggest that developmental bias may provide a focal point for the coming together of conceptual and practical approaches to evo‐devo.

The pattern of segment formation, as revealed by engrailed expression, in a centipede with a variable number of segments.

SUMMARY Arthropods vary enormously in segment number, from less than 20 to more than 200. This between‐species variation must have originated, in evolution, through divergent selection operating in ancestral arthropod species with variable segment numbers. Although most present‐day arthropod species are invariant in this respect, some are variable and so can serve as model systems. Here, we describe a study based on one such species, the coastal geophilomorph centipede Strigamia maritima. We investigate the way in which segments are formed using in situ hybridization to demonstrate the expression pattern of the engrailed gene during embryogenesis. We also analyze segment number data in mother–offspring broods and thereby demonstrate a significant heritable component of the variation. We consider how natural selection might act on this intraspecific developmental variation, and we discuss the similarities and differences in segment formation between the geophilomorphs and their phylogenetic sister‐group.

Latitudinal cline in segment number in an arthropod species, Strigamia maritima

Arthropods vary more than 30–fold in segment number. The evolutionary origins of differences in segment number among species must ultimately lie in intraspecific variation. Yet paradoxically, in most groups of arthropods, the number of segments is fixed for each species and shows no intra– or interpopulation variation at all. Geophilomorph centipedes are an exception to this general rule, and exhibit intraspecific variation in segment number, with differences between individuals being determined during embryonic development and hence independent of population age structure. Significant differences in segment number between different geographical populations of the same species have been previously reported, but insufficient sampling has been conducted to reveal any particular geographical pattern. Here, we reveal a latitudinal cline in segment number in the geophilomorph species Strigamia maritima: segment number in British populations decreases with distance north. This is the first such cline to be reported for any centipede species; indeed as far as we are aware it is the first such cline reported for any arthropod species. In vertebrates, fish are known to exhibit a latitudinal cline in segment number, but interestingly, this is in the opposite direction; fish add segments with increasing latitude, centipedes subtract them.

Effects of temporal priority on interspecific interactions and community development

The effects of temporal priority on interactions between the larvae of Drosophila hydei and D. melanogaster were investigated experimentally in the laboratory. In general, the species which arrived first at the resource had a competitive advantage, the extent of which was related to the length of the temporal separation between species introduction. A small or moderate temporal priority for one species tended to produce an unreciprocated inhibitory effect in the other and thus the interaction which occurred was highly asymmetric (amensal). However, if a species arrived very late at the resource it performed better if the resource had been previously utilized by larvae of the other species. This was due to amelioration of otherwise harsh conditions by the early-arriving larvae. Therefore, temporal priority can influence the direction, form and intensity of the interaction which occurs between two species. Due to the competitive advantage obtained when arriving first, competitively weak species may be able to persist in a community if they attain temporal priority on at least some patches of resource. However. in harsh conditions, arriving after another species may have positive effects due to a reduction in environmental stresses. The effects of temporal priority on interspecific interactions are therefore considered to be an important factor in the structuring of ecological communities.