Fishing for the Secrets of Vertebrate Evolution in Threespine Sticklebacks
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DEVELOPMENTAL DYNAMICS 234:815–823, 2005 REVIEWS—A PEER REVIEWED FORUM Fishing for the Secrets of Vertebrate Evolution in Threespine Sticklebacks Catherine L. Peichel* The threespine stickleback (Gasterosteus aculeatus) is rapidly emerging as a new model genetic system to study questions at the interface of evolution and development. The relatively rapid and recent diversification of this small teleost fish, combined with the development of genetic and genomic tools for this fish, provides an unprecedented opportunity to identify the genetic and molecular basis of morphological variation in natural populations of vertebrates. Recently, the genes underlying two different adaptive morphological traits in stickleback have been identified. This work has provided answers to four longstanding questions in the field of evolution and development: (1) How many genes underlie morphological variation in natural populations? (2) What are the genes that underlie morphological variation in natural populations? (3) Do coding or regulatory mutations underlie morphological evolution? (4) What is the molecular and genetic basis of parallel morphological evolution? Because stickleback populations also display natural variation in morphology, life history, physiology, and behavior, extending the approaches used to identify the genetic basis of morphological variation in sticklebacks to other phenotypes is sure to yield further important insights into the genetic and developmental basis of diversity in natural populations. Developmental Dynamics 234:815–823, 2005. © 2005 Wiley-Liss, Inc. Key words: threespine stickleback; genetics; evolution; pelvic reduction; plate morph Received 3 July 2005; Revised 22 July 2005; Accepted 26 July 2005 INTRODUCTION molecular pathways used to achieve THE THREESPINE the same phenotype? What are the mechanisms that under- STICKLEBACK AS A Many of these questions have chal- lie the variation of forms found in na- GENETIC MODEL SYSTEM lenged evolutionary biologists for over ture? Are the differences between spe- IN EVOLUTION AND a century. More recently, a number of cies due to the effects of many genes, DEVELOPMENT each with a small phenotypic effect, or researchers working at the interface can differences between species occur of evolution and development have Threespine sticklebacks (Gasterosteus as a result of mutations in genes with also begun to study these questions. aculeatus) are small teleost fish that large phenotypic effects? Are there In order to take a genetic approach to have been widely and intensively particular classes of genes that are answering these questions, it is neces- studied by ethologists, ecologists, and more likely to be modified to produce sary to identify natural populations evolutionary biologists, resulting in novel phenotypes? Do mutations in that have significant phenotypic vari- thousands of research papers and sev- these genes occur in protein coding ation, but can still be intercrossed in eral books on their morphology, phys- regions or regulatory regions? When the laboratory in order to identify the iology, life history, ecology, evolution, similar traits evolve in independent genetic and molecular mechanisms and behavior. Sticklebacks are widely populations, are the same genetic and that underlie morphological variation. distributed in both marine and fresh- Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington Grant sponsor: National Institute of General Medical Sciences; Grant number: GM71854; Grant sponsor: Burroughs Wellcome Fund; Grant number: 1003370. *Correspondence to: Catherine L. Peichel, Division of Human Biology, Fred Hutchinson Cancer Research Center, 1100 Fairview Ave North, Seattle, WA 98109. E-mail: [email protected] DOI 10.1002/dvdy.20564 Published online 26 October 2005 in Wiley InterScience (www.interscience.wiley.com). © 2005 Wiley-Liss, Inc. 816 PEICHEL water populations throughout the cis-regulatory elements that drive ex- (Baumgartner and Bell, 1984), para- northern hemisphere. The ancestral pression of genes in particular ana- site susceptibility (MacLean, 1980), sticklebacks are found in marine hab- tomical locations (DiLeone et al., increased body flexibility and changes itats and are relatively uniform in life 2000; Mortlock et al., 2003). With the in swimming performance (Taylor and history, morphology, and behavior. In development of many of these tools McPhail, 1986; Bergstrom, 2002), as contrast, the sticklebacks found in that were previously only available in well as changes in predation regime post-glacial freshwater lakes and more traditional model organisms, (Hagen and Gilbertson, 1973; Moodie streams have evolved a diversity of threespine sticklebacks are rapidly et al., 1973; Reimchen, 1992, 1995, morphologies, life histories, and be- emerging as a “supermodel” (Gibson, 2000) and climate (Hagen and Moodie, haviors from the ancestral marine 2005). 1982) have all been suggested as fac- form in response to local ecological Variation in skeletal armor, high- tors contributing to the evolution of conditions in a relatively short time lighted in Figure 2, is the most strik- lateral plate reduction. However, none scale of 12,000 years (Bell and Foster, ing phenotype found in natural popu- of these factors have been directly 1994). Despite this diversity, stickle- lations of sticklebacks. Marine proven to account for the repeated backs from virtually any two popula- sticklebacks are covered in bony ar- evolution of lateral plate morphs in tions from around the world can be mor, with three dorsal spines, two pel- thousands of freshwater populations crossed in the laboratory to generate a vic spines, and a continuous row of across the Northern hemisphere (Bell large number of viable and fertile bony lateral plates (Fig. 2A). The dor- and Foster, 1994). progeny, thereby facilitating the for- sal and pelvic spines (Fig. 2A) are Using a forward genetics approach ward genetic approach outlined in thought to be protective against gape- (Fig. 1), the genetic and molecular ba- Figure 1 to identify the molecular ba- limited predators, such as birds and sis of pelvic reduction and plate morph sis of natural phenotypic variation. piscivorous fish (Hoogland et al., 1957; variation has now been identified (Co- In order to identify the genes and Reimchen, 1983). However, several losimo et al., 2004; 2005; Cresko et al., molecular changes that underlie nat- freshwater populations from around 2004; Shapiro et al., 2004). This work ural variation, a variety of genetic and the world have evolved a complete or in sticklebacks has provided answers genomic tools are required. Despite partial loss of the pelvic skeleton (Fig. to some long-standing and fundamen- the long history of study in stickle- 2B), including sticklebacks from Pax- tal questions in evolutionary biology. backs, there were virtually no molec- ton Lake, British Columbia (Bell, In this review, I will frame each ques- ular or genetic tools available for this 1974), the Queen Charlotte Islands, tion in a historical context, briefly fish until a few years ago. There are British Columbia (Moodie and Reim- summarize some relevant work in now hundreds of microsatellite mark- chen, 1976; Reimchen, 1984), Quebec other taxa, and then describe the re- ers available, which are distributed (Edge and Coad, 1983), the Cook Inlet cent work in sticklebacks and its rel- across the genome and have been or- region of Alaska (Bell et al., 1993), evance to these questions. I will end dered into a genetic linkage map for southern California (Bell, 1987), the by discussing some of the future re- use in genetic linkage analysis in vir- Outer Hebrides in Scotland (Camp- search directions that can be taken in tually any stickleback population bell, 1979, 1985), and Iceland (Shapiro this newly emerging model for inte- (Peichel et al., 2001). Several bacterial et al., 2004). It has been hypothesized grative research in evolution and de- artificial chromosome (BAC) libraries that loss of pelvic structures in stick- velopment. have been constructed to facilitate po- lebacks could be the result of the ab- sitional cloning of genetic loci identi- sence of predatory fish, reduced levels fied by genetic linkage analysis of calcium availability, or predation by HOW MANY GENES (Kingsley et al., 2004). Nearly 100,000 macroinvertebrates (Reimchen, 1980, UNDERLIE ESTs from a variety of tissues and 1983; Reist, 1980a,b; Giles, 1983; Bell MORPHOLOGICAL developmental stages have now been et al., 1993; Ziuganov and Zotin, VARIATION IN NATURAL deposited in GenBank, and provide a 1995), although none of these hypoth- POPULATIONS? resource for the cloning of interesting eses can completely account for all candidate genes (Kingsley et al., cases of pelvic reduction. Does evolution proceed via the accu- 2004). Expression patterns of these The most commonly observed mor- mulation of small changes with minor candidate genes can be assayed using phological variation in freshwater phenotypic effects or can mutations of in situ hybridization (Ahn and Gibson, sticklebacks is a reduction in the num- large phenotypic effect underlie evolu- 1999a, 1999b; Cresko et al., 2003; ber of lateral plates (Fig. 2B). Most tionary change? This question has Shapiro et al., 2004; Tanaka et al., marine sticklebacks, although not all been debated since the time of Dar- 2005). Transgenic technologies have (Klepaker, 1996), have a complete set win, and Darwin himself believed that also been developed for sticklebacks of lateral plates along their side