Comparative genetics of postembryonic development as a means to understand evolutionary change

Abstract

Summary This review addresses the use of comparative studies of development to help understand the mechanisms underlying the evolution of morphological and physiological diversity. Mutation analysis in experimental model organisms is at the core of our understanding of how development works, and these findings have proven important in the identification and functional support of genetic variations associated with character change in natural populations. However, it has been argued that the essential and pleiotropic effect of many developmentally important genes limits the utility of such mutational study of development toward understanding evolution. Here, I argue that an analysis of the genetic regulation of postembryonic development will refine such comparative analysis. By focusing on late developmental events, one limits the type of genes as well as the types of genetic and developmental changes that may underlie evolutionary change. This may refine the predictive value of such comparative analysis. In this review, I discuss the use of fish as experimental and natural models to address these questions. Fish have several established, experimental models for genetic analysis. Additionally, the morphological and genetic diversity among fish provides a wealth of new models in which to look at the genetic and developmental basis of character change. This broadening of comparative genetic analysis may resolve the bias against genetic ‘monsters’ and what they can tell us about evolutionary change.

Metamorphosis in Teleosts

“…Moreover, this period of coordinated tissue modification offers the opportunity to examine differential tissue responses to global endocrine signals. Genetic modifications to these postembryonic processes have contributed to the spectacular diversity in adult morphology seen within teleost lineages, and elucidating their attendant molecular mechanisms will lend considerable additional insight into this diversification (Harris, 2012). Although the weight of evidence supports roles for TH signaling in promoting metamorphosis in teleosts, roles for other factors remain likely but uncertain, and the precise mechanisms by which TH effects particular morphogenetic or physiological outcomes remain largely unknown.…”

Endoskeleton/Exo (dermal) skeleton - Mesoderm/Neural Crest: Two pair of problems and a shifting paradigm

“…In zebrafish ( Danio rerio ), initiation of these segments, addition of new segments, and control of segment length are regulated independently during growth of the caudal fin (Laforest et al., ) – which is isometric with growth of the body – as demonstrated by analysis of two mutants, short fin ( sof ), in which segment number and segment size are both reduced, and long fin ( lof ), which allows additional segmentation of fin rays (Iovine and Johnson, ). Patterning of the fin rays also is under the influence of Shh , Patched1 , Bmp2 and members of other gene families (Harris, ); Evx1 , a member of the even skipped gene family, is expressed at sites of future joints and segment boundaries in zebrafish caudal and pectoral fins during development and regeneration (Borday et al., ).…”

“…() turned to another teleost, the Japanese medaka Oryzias latipes to investigate the cellular origin of the fin rays and scales. Scales, which come in an abundance of types, compositions, and responses to agents such as hormones, form an important body covering for teleost fishes (Harris, ; Witten et al., ). They provide protection for the body (especially for such superficial organs as the lateral lines), a barrier between organism and environment and against infection, and a source of Ca 2+ and PO 4 3− that can be mobilized by resorption and influenced by hormones (Levin and Levina, ).…”

Interdisciplinary approaches in fish skeletal biology

“…Through the long list of species examined by Melvin Moss, we obtained an idea about the enormous diversity of fish bone structures. A major task of today’s research is to place this variety in an evolutionary frame, be it on the morphological, the developmental or the genetic levels (Hall, 2010; Huysseune et al., 2010; Wilga, 2010; Gillis et al., 2012; Harris, 2012; Mabee et al., 2012; Milligan et al., 2012).…”

“…Despite the huge diversity of fish species and fish skeletal tissues, today we increase our knowledge about fish skeletal development and the underlying genetics by focusing on two small teleosts, which have become models for developmental and biomedical research: zebrafish ( Danio rerio ) and Japanese medaka ( Oryzias latipes ) (MacDonald et al., 2010; Schilling et al., 2010; Spoorendonk et al., 2010; Gorman et al., 2012; Germanguz and Gitelman, 2012; Harris, 2012; Renn and Winkler, 2012). In addition, further teleost models emerge.…”