Integrative and Comparative Biology Advance Access originally published online on March 29, 2006
Integrative and Comparative Biology 2006 46(3):233-242; doi:10.1093/icb/icj030
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The evolution of embryonic gene expression in sea urchins
Department of Biology, Duke University Box 90338, Durham, NC 27708-0338, USA
Correspondence: 1E-mail: gwray{at}duke.edu
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Synopsis |
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Many evolutionary modifications in development and life history derive from changes in embryonic gene expression. However, the genetic variation affecting gene expression in natural populations is not well understood, nor are the evolutionary mechanisms that operate on that variation. The early embryonic gene network of the purple sea urchin (Strongylocentrotus purpuratus) has been studied in considerable detail, providing an informative basis for analyzing the developmental and evolutionary mechanisms that alter gene expression. Comparative functional analyses have been carried out for several genes. These case studies indicate a complex relationship between sequence divergence and gene expression: in some cases, gene expression is conserved despite extensive divergence in cis-regulatory sequences, while in others the basis for a change in gene expression does not reside locally but rather in the expression or activity of transcription factors that regulate its expression. Diverse evolutionary mechanisms apparently operate on cis-regulatory regions, including negative, balancing, and stabilizing selection.
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Introduction |
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Marine invertebrates have evolved a dazzling array of life histories. Two general properties of these life histories remain particularly striking, even though they have been well known for more than a century. One is the degree of anatomical disparity between larvae and adults; the other is the degree to which life histories can differ among related species (McEdward 1995
). These phenomena raise some obvious evolutionary and ecological questions. Why do larvae look so different from their adult counterparts (some to a rather extreme degree), in so many species from so many different phyla? And why have such distinct life histories evolved so often, in some cases between closely related species whose adults are anatomically similar?
At a general level, we understand why so many marine invertebrates have complex life histories and why these life histories encompass so much diversity. The answer is that the manner in which an organism develops is just as important as the adult phenotype it produces (Garstang 1922; McEdward 1995; Wray 2002). Development must not only construct a reproductively competent adult, but it must do so in a way that is compatible with survival. Much, perhaps most, of the disparity among life history phases and the diversity between taxa that exists in marine invertebrate life cycles is driven by ecological circumstances. Larvae look different from adults because their food, predators, and physical environment are so distinct; related species develop in different ways because of life history trade-offs between fecundity, maternal provisioning, dispersal, and stage-specific mortality.
In contrast, we know much less about how life histories evolve in marine invertebrates (Hart 2002; Wray 2002). The developmental and genetic bases for life history transitions have been studied in the greatest detail within 2 groups, the echinoid genus Heliocidaris (for example, Raff 1992; Kauffman and Raff 2003) and the ascidian genus Molgula (for example, Swalla and others 1993; Swalla and Jeffery 1996), where a few of the relevant genes and developmental processes have been identified. For most other life history transitions in marine invertebrates, there is very little developmental or genetic information. We know even less from the perspective of population genetics: what kind of genetic variation has an impact on life histories, how much of it there is in natural populations, and how natural selection operates on this variation. This review considers how evolutionary changes in development can arise from the perspectives of developmental and population genetics, with a focus on the early development of sea urchins.
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Genetic markers and genetic causes |
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Gene sequences contain many kinds of information about evolution. One general approach utilizes genes as passive markers carried by organisms. Genes accumulate mutations over time that can be used to track several kinds of evolutionary processes and to reconstruct phylogenetic relationships (Avise 2004
). This use of genes as markers has been enormously successful. It forms much of the empirical material of modern population genetics, conservation genetics, and phylogenetics. A second general approach examines the natural history of genomes. This approach analyzes processes of change in specific components of genomes, such as gene duplication, rates of sequence substitution in introns versus exons, and the dynamics of mobile elements (Li 1997). This is the domain of traditional studies in molecular evolution. It, too, has been enormously successful, and has produced a detailed understanding of how the key processes of mutation, drift, and selection operate differently in distinct components of a genome. A third general approach to studying evolution at a genetic level views genes as the basis for particular phenotypes. Two groups of biologists have taken this approach: developmental biologists and evolutionary geneticists (Wilkins 2002). Although they have operated largely independently of each other and have pursued ostensibly distinct research agendas, both groups have worked to identify which genes contribute to specific aspects of phenotype and how specific mutations in these genes differ in their effects. This research has provided a general understanding of how mutations can, on the one hand produce, and on the other have produced, phenotypic change at an organismal level.
Of these 3 approaches, the first has so far contributed the most to understanding the evolution of life histories of marine invertebrates. A clearer understanding of phylogenetic relationships has helped to reconstruct the history of life history transformations and to clarify the evolutionary mechanisms that have operated on them (Strathmann and Eernisse 1994; McEdward and Miner 2001; Hart 2002). For some clades, it has been possible to infer ancestral life history states and to estimate how many times parallel changes in life histories have evolved (Wray 1996; Rouse 1999; Huber and others 2000). Genetic markers have also provided a way to compare levels of gene flow and effective population size in species with different life history modes (MacMillan and others 1992; Arndt and Smith 1998; Bohank 1999) and to track macroevolutionary trends such as speciation and extinction rates (Duda and Palumbi 1999; Jeffery and others 2003). From these studies, it is clear that life history modes are evolutionarily labile, at least within some phyla, and that changes in life history mode can have a significant impact on subsequent evolution through its effects on the genetic structure of populations.
The second of the 3 broad approaches has contributed to understanding life history evolution only in an indirect way. This is because traditional approaches to molecular evolution generally ignore the phenotypic consequences of mutations and are concerned instead with understanding their general evolutionary dynamics. For instance, this approach has provided a detailed understanding of how the consequences of mutations differ, depending on precisely where they occur within a gene. Some of this information has been gathered from marine invertebrates (for example, Britten and Davidson 1971; Biermann 1998; Balhoff and Wray 2005), but most of it is based on other groups of organisms.
The third broad approach has tremendous potential to illuminate our understanding of life history evolution in marine invertebrates, but has not been utilized extensively. A few studies have demonstrated the power of this approach, by focusing attention on evolutionary changes in the embryonic expression of genes that may have contributed directly to a change in life history. A dramatic example is the Manx gene of ascidians, whose expression differs in 2 closely related species of Molgula with tailed and tailless larvae (Swalla and Jeffery 1996). Manx protein is a tyrosine kinase that plays an important role in establishing the notochord during ascidian development, and its absence in embryos of M. occulata is probably an important part of the reason this species lacks a larval tail. The sea urchin genus Heliocidaris, which contains species with feeding and nonfeeding larvae, provides another example. The timing and spatial expression of many genes expressed during embryonic and larval development differs between the 2 species (for example, Parks and others 1988; Kissinger and Raff 1998; Ferkowicz and Raff 2001). Some of these changes in gene expression profiles appear to be causally related to the evolution of the anatomically simplified larva of Heliocidaris erythrogramma (Kauffman and Raff 2003; Zhou and others 2003; Wilson and others 2005).
These studies have uncovered specific genes that contributed to evolutionary changes in life history in Molgula and Heliocidaris. In both cases, modifications in gene expression were important. There is growing evidence that changes in gene expression are often an important part of the basis for phenotypic evolution. Although this idea dates back to the early days of molecular evolution (Wilson 1975), only in the past few years have clear cases emerged. Examples include color patterns on butterfly wings (Brakefield and others 1996; Brunetti and others 2001; Beldade and others 2002), armor reduction in sticklebacks (Peichel and others 2001; Shapiro and others 2004), and beak size increase in Galapagos finches (Abzhanov and others 2004). In all of these cases, and in many others, a spatial or temporal change in gene expression was a key part of the basis for an ecologically significant change in organismal phenotype (Wray and others 2003). Indeed, some authors have argued that changes in gene expression are overall at least as important as changes in gene function in the evolution of organismal phenotypes (Carroll 2000; Stern 2000; Davidson 2001; Wilkins 2002).
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Studying the evolution of gene expression |
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But how do changes in gene expression actually evolve? Despite the significance of this question, we are only beginning to understand the genetic, molecular, and evolutionary causes that are involved.
One point that is fairly well established is that evolutionary differences in gene expression are common, both within populations and between species. Estimating the frequency of evolutionary changes in gene expression presents some unique challenges, since expression can vary over time, in different cell types and regions of the body, and in response to diverse environmental conditions. Because it is difficult to examine all possible aspects of an expression profile, evolutionary surveys of gene expression can only provide minimum estimate of the number of differences. Nonetheless, evolutionary differences are not hard to find. Several studies have surveyed quantitative differences in gene expression within populations and between in closely related species (for example, Jin and others 2001; Cowles and others 2002; Enard and others 2002; Oleksiak and others 2002; Schadt and others 2003; Rifkin and others 2003; Morley and others 2004). Most of these quantitative comparisons examined thousands of genes, and were consequently able to provide firm minimum estimates of the fraction of genes whose expression varies in this way. Fewer studies have surveyed spatial patterns of gene expression; for practical reasons, this is currently not feasible on a large scale, and most studies examined 1 or a few loci. As expected, spatial expression patterns are sometimes conserved (Sommer and Tautz 1991), but a surprising number show changes (Wray and McClay 1989; Sommer and Tautz 1991; Ross and others 1994; Swalla and Jeffery 1996; Brunetti and others 2001).
An issue that needs much more work is how different evolutionary mechanisms operate on cis-regulatory sequences, also known as promoters (sensu lato). There is a general expectation that cis-regulatory sequences should be maintained by negative selection because they are functionally important. On the one hand, many studies have detected sequence conservation within cis-regulatory regions that is consistent with negative selection; on the other, many functionally important cis-regulatory sequences are not conserved (reviewed by Wray and others 2003). An important challenge for the future will be understanding the relative contributions of drift and various kinds of selection (positive, negative, balancing) to the evolution of cis-regulatory sequences. Part of the problem is that cis-regulatory sequences cannot be identified without functional and biochemical studies, so it isn't clear in most cases which nucleotides are functionally important and which ones are not.
Identifying the genetic basis for evolutionary differences in gene expression presents another challenge, mainly because there are so many places to look (Fig. 1). The mutation could lie within the cis-regulatory region of the gene itself, in the coding sequence of any of the transcription factors that interacts with its cis-regulatory sequences, or in any of the cis-regulatory regions of any of these transcription factors. The mutation could even lie in any of the transcription factors that interact with these cis-regulatory regions. Literally dozens of loci could potentially harbor a mutation that changes the expression of any particular gene. This difficulty is compounded by the fact that cis-regulatory sequences are not organized in a consistent manner: transcription factor binding sites can lie within the introns of a gene or within several kb 5' or 3', and are often separated by long stretches of apparently non-functional sequence; in some cases regulatory sequences lie within introns of adjacent genes or on the other side of them (Wray and others 2003). Together, the prevalence of cis/trans interactions and the lack of a consistent spatial organization to cis-regulatory sequences pose a challenge when searching for evolutionary changes that might affect gene expression. Fortunately, the genetic basis for many gene expression differences resides within cis-regulatory sequences (Stern 2000; Wray and others 2003). This makes it possible to begin locating and analyzing the effects of specific mutations that influence gene expression, but the possibility of additional genetic factors influence gene expression elsewhere in the genome can never be ruled out.
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Sea urchins have proven to be an unusually useful group for studying the evolution of gene expression, and are now one of the best-studied taxa in this regard. The organization of function of many cis-regulatory sequences has been studied in considerable detail in the purple sea urchin, Strongylocentrotus purpuratus (Davidson 2001
; Oliveri and Davidson 2004). This knowledge base partially alleviates the problem of missing information, by delineating which sequences within a cis-regulatory region are functional. Echinoid development has also been studied extensively by larval ecologists and evolutionary biologists (Smith 1997; Strathmann 2000; Hart 2002), which provides an important context for understanding how selection operates on anatomy and life history. Finally, the phylogenetic relationships and divergence times of echinoids are relatively well understood, due to their unusually good fossil record and recent efforts by molecular phylogeneticists (Smith and others 1995; Jeffery and others 2003; Biermann and others 2003). |
Gene expression and life history evolution: MSP130 |
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The msp130 locus encodes a structural glycoprotein that is a component of the endoskeleton in echinoderms (Anstrom and others 1987
). The expression of msp130 has been examined in 10 sea urchin species, and in all cases transcription is restricted to a single cell type, the skeletogenic cells. However, the timing of initial expression differs. In species with planktotrophic development, the onset of msp130 expression occurs as skeletogenic cells ingress or during their subsequence migration, but always before they reach their destination and begin synthesizing skeleton (Wray and McClay 1989). In echinoids with lecithotrophic development, the larval skeleton is greatly reduced and skeletogenesis delayed. In 3 such species, representing 3 independent transitions from planktotrophy to lecithotrophy, the onset of msp130 expression is considerably delayed (Parks and others 1988, 1989; Amemiya and Emlet 1992).
These changes in the timing of msp130 expression may be the result of several evolutionary processes (Wray and Bely 1994; Wray 1996). In species with planktotrophic larvae, relatively small changes in expression probably don't have a fitness consequence since they involve relatively minor modifications in timing prior to the time the protein is actually needed. Although these changes may accumulate by drift, the scope for variation is likely limited by negative selection to a window of several hours: later onset in particular would delay synthesis of the larval skeleton, which would slow feeding and growth, with likely adverse fitness consequences. In species with lecithotrophic larvae, in contrast, the larval skeleton is no longer required for feeding. Under these circumstances, the scope for neutral changes in msp130 expression is likely to be much broader, since delaying skeletogenesis would have no impact on larval growth. The phylogenetic correlation between a large delay in the onset of msp130 expression and lecithotrophic larvae is statistically significant (Wray and Bely 1994), suggesting that the change is not random and that directional selection may have favored variants producing later expression.
In one of these cases, the genetic basis for the delay in onset of expression has been examined experimentally. Klueg and colleagues (1997) compared the cis-regulatory region of H. erythrogramma, which has a lecithotrophic larva and delayed onset of msp130 expression, to those of Heliocidaris tuberculata and S. purpuratus, both of which have planktotrophic larvae. In all 3 species, about 200 bp of 5' flanking sequence is evolutionarily conserved, corresponding to just a fraction of the 
1.1 kb cis-regulatory region in S. purpuratus. The function of the msp130 cis-regulatory region from H. erythrogramma was tested in the embryo of another species with planktotrophic larvae (Lytechinus pictus), where it produced early expression (Klueg and others 1997). This result suggests that the genetic basis for the delay in onset of msp130 expression in H. erythrogramma is not due to mutations in its cis-regulatory region (possibility 1 in Fig. 1), but rather to changes in the expression or function of the transcription factors that interact with it (possibilities 2, 3, or n in Fig. 1). The heterochrony in msp130 transcription illustrates a simple but important distinction between the evolution of proteins and the sequences that regulate their expression: mutations affecting the function of a protein reside almost exclusively in cis, while those affecting its expression can reside in cis or in trans—and both situations are common.
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Turnover of cis-regulatory sequences: SPEC2A |
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The spec2a locus provides an instructive example of the complex interaction between cis-regulatory sequence and function. This locus is part of a small gene family that encodes intracellular calcium-binding proteins. The spec2a paralogue is expressed in an essentially identical pattern within the larval aboral ectoderm in several sea urchin species (Brandhorst and Klein 1992
). Despite this conservation of expression, the cis-regulatory sequences that regulate transcription are quite different between L. pictus and S. purpuratus (Xiang and others 1991), which diverged about 35–40 million years ago (Smith 1988). This situation is apparently a rather common feature of cis-regulatory sequence evolution, with many other examples now known (for example, Piano and others 1999; Ludwig and others 2000; Dermitzakis and Clark 2002; Romano and Wray 2003; Ruvinsky and Ruvkun 2003). The usual interpretation in such cases is that stabilizing selection operates on the expression profile, and turnover of transcription factor binding sites is possible because of functional redundancies.
In the case of spec2a, some of the specific sequence differences and their functional consequences have been identified. One clear functional difference is the presence of a repetitive element named RSR that is present in the 5' flanking region of several members of the spec gene family in several species in the family Strongylocentrotidae but are apparently absent from the spec paralogues in Lytechinus. RSR functions as a transcriptional activator in at least 3 of the spec paralogues in S. purpuratus (Gan and others 1990). The polarity of the change is not known (that is, whether RSR was lost in Lytechinus or gained in Strongylocentrotus), since no outgroups have been examined.
For a second set of functional changes in the spec2a promoter, however, the polarity is clear. Two single base substitutions that generated new transcription factor binding sites are uniquely present within the RSR element of the spec2a element in S. purpuratus, and represent a derived condition (Dayal and others 2004). One single base substitution generates a binding site for a CCAAT-binding protein, while the other generates a binding site shared by 3 proteins: Orthodenticle, Goosecoid, and ETS-4. Careful functional tests have demonstrated that both of these new transcription factor binding sites are necessary for producing the correct spatial, temporal, and quantitative transcription of spec2a in S. purpuratus. Evidently, other binding sites, as yet unknown, carry out similar functions in other sea urchin species, since the transcription of spec2a is well conserved.
This phenomenon of binding site turnover is apparently quite common. Because transcription factor binding sites are short, partially degenerate, and to a large extent position and orientation independent, new sites can appear through processes of random substitution at an appreciable rate (Stone and Wray 2001; MacArthur and Brookfield 2004). Many cases have been discovered (for example, Piano and others 1999; Ludwig and others 2000; Romano and Wray 2003; Ruvinsky and Ruvkun 2003), although few have been functionally tested at the level of detail of spec2a. A survey of polymorphic binding sites in humans found that more than one third represented gains of new transcription factor binding sites (Rockman and Wray 2002). The picture of cis-regulatory sequence evolution that is emerging is one of dynamic change at the level of sequence comparison, coupled with long-term conservation in the gene expression profile.
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Evolutionary mechanisms and cis-regulatory sequences: ENDO16 |
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SynopsisIntroductionGenetic markers and genetic...Studying the evolution of...Gene expression and life...Turnover of cis-regulatory... Evolutionary mechanisms and cis... Future directionsReferences |
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The cis-regulatory region of endo16 is one of the most thoroughly analyzed and best understood of any metazoan gene. Detailed studies over the past decade have produced an exceptionally complete and detailed understanding of the organization of binding site sequences and function (Yuh and others 1994
, 1996, 1998, 2001; Yuh and Davidson 1996). This work has identified 7 functional modules (A–G), each of which contains a cluster of transcription factor binding sites and each of which has a distinct role in generating the overall transcription profile. endo16 encodes a large, extracellular protein (Nocente-McGrath and others 1989) that probably functions in cell adhesion during gastrulation (L. Romano and G. Wray, manuscript submitted). Transcription is restricted to the archenteron during gastrulation and the midgut of the larva in S. purpuratus (Ransick and others 1993), and differs only slightly in Lytechinus variegatus (Romano and Wray 2003).
An analysis of the population genetics of the endo16 cis-regulatory region reveals conspicuous regional differences in genetic variation across 3 kb that correlate with the function of regulatory modules (Balhoff and Wray 2005). The 2 most proximal modules, A and B, are the only ones that can activate transcription; modules C–F are responsible for repressing transcription outside the endoderm; and module G is a weak booster element (Yuh and Davidson 1996). Consistent with this functional organization, modules A and B contain the lowest levels of genetic polymorphism (Fig. 2A). This result suggests that the intensity of negative selection can differ within subcomponents of a cis-regulatory region and that mutations in sequences required for activation are more likely to have fitness consequences than mutations in sequences required for repression. Both conclusions fit expectations based on the way cis-regulatory regions function (Wray and others 2003).
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A counterintuitive finding, on the other hand, is that genetic variation is higher within binding sites than flanking sequences. Transcription factor binding sites are the functional components of a cis-regulatory region, and one might expect that negative selection would conserve their sequences relative to the surrounding non-functional sequences. Such is not the case over most of the endo16 cis-regulatory region: only in module A is genetic variation significantly reduced in binding sites, while elsewhere it is actually higher (although not significantly so). One possibility is that balancing selection maintains polymorphisms. S. purpuratus, like many sea urchins with planktotrophic larvae, has a broad geographic distribution and extensive gene flow (Palumbi and Wilson 1990
). In the case of S. purpuratus, the range extends across more than 20° of latitude and includes a great diversity of local habits (Jensen 1974). If some cis-regulatory variants are favored by geographically heterogeneous selection, the combination of local adaptation and extensive gene flow could maintain polymorphisms in the population at large.
A striking feature of sequence variation within the endo16 cis-regulatory region is the presence of a large (350 bp) insertion that is segregating at a low frequency. This insertion, which is present in the cis-regulatory haplotype that was characterized by Yuh and colleagues (1996 and later papers), contains nearly all of 2 modules (E and F) and functions as a strong ectodermal repressor. However, most haplotypes segregating in the wild lack this insertion (Balhoff and Wray, 2005). Other sequences within the endo16 cis-regulatory region must function to restrict ectodermal expression in most haplotypes. This insertion demonstrates that transposition can introduce fairly large pieces of DNA containing multiple transcription factor binding sites into an already functional cis-regulatory region. Such mutations are much rarer than point mutations, but may have a significant impact on promoter evolution over longer time scales (Wray and others 2003).
Interspecific comparisons of the endo16 cis-regulatory sequence parallel the spatial structuring of genetic variation within populations. In a comparison with a closely related species, Strongylocentrotus droebachiensis, the most conserved regions are once again the 2 activator modules A and B (Fig. 2B), suggesting that negative selection has operated to maintain these sequences over much longer timescales than are apparent from the population comparisons alone. Another parallel between intra- and interspecific sequence evolution is evident in comparisons between binding sites and flanking nucleotides; again, binding sites are not preferentially conserved, except in module A. S. purpuratus and S. droebachiensis diverged about 5 million years ago (Biermann and others 2003; Lee 2003), so this scale of comparison is informative about relatively recent interspecific changes in cis-regulatory sequence.
A more distantly related species, L. variegatus, diverged about 35–50 million years ago (Smith 1988), providing a view of cis-regulatory sequence dynamics over a much longer term. At this scale, the cis-regulatory region of endo16 is still moderately well conserved in module A, poorly conserved in module B, and so divergent that it cannot be aligned in the other modules (Fig. 2C) (Romano and Wray 2003). Despite this degree of divergence in sequence, the function of the cis-regulatory region has been maintained: in both species, 2 kb of 5' flanking sequence is sufficient to drive expression of a reporter that replicates the expression profile of the endogenous endo16 gene. Reciprocal experimental swaps of the cis-regulatory regions drive nearly perfect expression in the opposite species, indicating that many of the transcription factors that interact with the endo16 cis-regulatory region are expressed in conserved domains within the embryo. Some ectopic expression also occurs from the S. purpuratus cis-regulatory region in L. variegatus embryos, suggesting that the sequences regulating repression function somewhat differently in the 2 species. Taken together, these results indicate that functional changes have evolved in both the cis-regulatory region of endo16 and in the transcription factors that interact with it.
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Future directions |
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One of the major intellectual challenges in studies of molecular evolution is understanding how changes in gene expression take place in natural populations, how these changes affect organismal traits, and which ecological circumstances promote or permit these changes. Sea urchins have provided a number of valuable insights into these processes, and provide a powerful system for further study. A particularly promising avenue for future research will be placing the most thoroughly characterized developmental gene network of any marine invertebrate (Levine and Davidson 2005
) into a substantive larval ecology and population genetic framework. It will be interesting to learn how much this gene network differs among and within species. Some of the first hints have begun to emerge, through comparisons at distant (Hinman and others 2004) and more recent (Romano and Wray 2003; Balhoff and Wray 2005) evolutionary time scales. Another productive area will be investigating "natural experiments" in life history evolution, particularly those represented by species with lecithotrophic development (Raff 1992; Wray 1996). These ecologically significant cases involve extensive modifications in gene expression (for example, Kissinger and Raff 1998; Ferkowicz and Raff 2001; Wilson and others 2005), but it is not yet clear why most of these changes have evolved. In the long term, an important goal will be building an understanding of the evolution of gene expression that reaches from genetic bases, through biochemical consequences and organismal phenotypes, to their broader ecological and macroevolutionary contexts; it is only through these connections that we can begin to address the full complexity of the evolution of gene expression.
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Acknowledgements |
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Thanks to James Balhoff, William Nielsen, Matt Rockman, Laura Romano, and Ann Rouse for stimulating discussions. Research in my lab is supported by the NSF and NASA.
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Footnotes |
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From the symposium "Complex Life-Histories in Marine Benthic Invertebrates: A Symposium in Memory of Larry McEdward" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2005, at San Diego, CA.
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