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Are Genome Evolution, Organism Complexity and Species Diversity Linked?1
1 Department of Biology, East Carolina University, Greenville, North Carolina 27858-4353
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Fishes represent an extremely diverse group of vertebrates with a deeply rooted evolutionary history. An understanding of their biology is being enriched by advancements in phylogenetic analysis and genomics, which are providing the framework for deciphering their evolutionary relationships and the molecular details that govern their evolution. Recent discoveries about the structure and function of fish genomes suggest the occurrence of large-scale genome level duplications within the stem lineage of the Actinopterygii (ray-finned fishes). However, little is understood about the effects, if any, of this event in relation to organismal complexity or species diversity. In this manuscript, I propose a hypothesis to test whether there is a likely relationship linking vertebrate genomes, organisms and species diversity. In so doing, I discuss the problems inherent in defining the complexity of genomes and organisms and provide simplifying assumptions that enable a preliminary test of the hypothesis. Results of this test suggest the likelihood of linkage between large-scale genome changes and organismal complexity early in vertebrate evolution but not in the evolution of the ray-finned fishes. A particularly interesting implication of the results is that there may be a limit to the effects of genome level duplications on organismal complexity and species diversity.
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An examination of the patterns and processes involved in the evolution of the actinopterygians (ray-finned fishes) requires an analysis of the genomic evolution accompanying biological change in this vastly divergent and highly successful vertebrate group. Of particular interest in this regard, is the influence of genome evolution on organism complexity and speciation. It has become commonplace to read that speciation in ray-finned fishes is unmatched among descendants of the other major vertebrate lineage, the sarcopterygians (Amores et al., 1998
; Meyer and Schartl, 1999; Taylor et al., 2001). Provided that the actinopterygians did indeed speciate more extensively than the sarcopterygians, it seems reasonable to ask if there are discernable features related to the evolution of fish genomes that intimate the underlying nature of the molecular processes driving this divergence?
In 1998, Amores and colleagues (1998) published a manuscript describing the Hox cluster organization of the zebrafish (Danio rerio) in which they demonstrated unequivocally, that this cypriniform fish possesses an outsized number of Hox clusters relative to mammals. In their manuscript, they argued "that teleosts, the most species-rich group of vertebrates, appear to have more copies of these developmental regulatory genes than do mammals, despite less complexity in the anterior-posterior axis." Their observation that Hox cluster complexity in teleosts appears to be independent of organismal complexity contradicts the consensus that chordate Hox cluster, genome, and organismal complexity increase in parallel (Holland, 1999). As an explanation for this apparent disjunction, they hypothesized that the increased Hox gene complement of ray-finned fishes likely contributed in some fashion to species diversification but presumably not organismal complexity. The implication being that the duplication propagated species diversification rather than organismal innovation. Based on the presumption that Hox cluster duplications were indicative of a total genome duplication event unique to early actinopterygian evolution, Meyer and Schartl (1999) broadened Amores's hypothesis by proposing that genome duplication not just duplication of Hox clusters drove species diversification in actinopterygians (Fig. 1). While these hypotheses are appealing to those who advocate genome duplications as a driving force in the evolution of organismal novelty, it leaves open the question of why a duplication within the stem lineage of the Actinopteryii, unlike similar deeply rooted vertebrate genome duplications, may have fueled species diversification in the apparent absence of a concordant increase in organism level complexity? A related but more fundamental question is whether large-scale genetic duplications consistently presage or parallel advancements in organism complexity, whether they fuel diversification, or if they generally do both or neither?
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Although genome duplications are less common among vertebrates than within other major taxonomic groups, most notably the plants, there is a growing body of evidence to support that genome level or at least large-scale duplications have occurred repeatedly in vertebrate evolutionary history (Gibson and Spring, 2000
; Taylor et al., 2001; Furlong and Holland, 2002; Gu et al., 2002; McLysaght et al., 2002). Interestingly, these large-scale vertebrate duplications, roughly defined as those occurring prior to the divergence of the actinopterygian and sarcopterygian lineages (Fig. 1), seem to correlate well with accepted notions of increasing organism complexity, and arguably occur concurrently with the extensive species diversification characteristic of vertebrates (Durrand, 2003). This correlation of large-scale genetic duplication, organism complexity and species diversification is indicative of a coordinated relationship linking vertebrate genomes, organisms and their capacity for diversification. If such a correlation exists, it might be expected that large-scale genetic shifts, particularly those that trace back to ancient polyploidizations would have similar effects. However, this seems not to be the case. Genome duplications that have occurred more recently than those that marked the inception of the vertebrates, e.g., within the stem lineage of the ray-finned fishes as well as within more restricted teleost lineages, seem relatively unremarkable in relation to their apparent influence on organismal innovation. If there is a discrepancy in the relationship between large scale genome shifts, organism complexity and species diversification at different times in vertebrate evolution what might be the reason for the differences? A possible explanation is a differential effect in which the duplication events that occurred earlier at a time when vertebrates were less complex promoted innovation and diversification whereas later events that occurred when overall organismal complexity was greater were ineffectual or extremely limited in effect. This explanation is valid under the premise that evolutionary innovation and species diversification may have inherent limits, which would generate an apparent time-dependent plateau in innovation and diversification.
The earliest genome duplication events are hypothesized to have occurred at the inception of the vertebrates as they evolved from their chordate ancestors (Holland et al., 1994; Sidow, 1996). This was a time when vertebrates were arguably less complex than their descendants. More recent duplications, particularly the duplications hypothesized to have occurred early in the actinopterygian lineage and again in the salmonid and catostomid lineages may have failed to usher in a similar period of developmental and morphological innovation (Taylor et al., 2003; Bailey et al., 1978).
An alternative explanation is that these temporally distinct genome shifts are equally effective but that insufficient time has elapsed since the occurrence of the more recent duplications, which date between 320– 450 mya for actinopterygians (Kumar and Hedges, 1998; Chiu et al., 2004; Vandepoele et al., 2004) or 40–70 mya for salmonids (Hartley, 1987), and the expression of their "evolutionary potential." Initial estimates indicate that the linkage between the earliest vertebrate duplications and advancements in organismal innovation is relatively tight, i.e., within tens of millions of years (McLysaght et al., 2002). This estimate correlates well with the measured 4 million year half-life of duplicated genes (Lynch and Conery, 2000), an estimate that suggests functional differentiation leading selection to maintenance of duplicated genes resulting from genome level duplications must occur within tens of millions of years rather than hundreds of millions of years. If correct these results suggest that the 320–450 million years since the proposed actinopterygian duplication is sufficient time to observe an effect on organismal innovation and species diversification or for the duplicated genes to vanish into oblivion. Yet another scenario is that large-scale vertebrate duplications are unlinked to organismal innovation or species diversification and that the observed differences are stochastic and ineffectual. This explanation requires that some genetic or epigenetic system other than gene duplication is responsible for fueling the observed innovations and species diversification. Unlike invertebrates, the general gene expression systems of vertebrates appear to be shared widely, including a vertebrate-specific global genome methylation system, indicative that in vertebrates, at least, epigenetic systems suitable to account for vertebrate innovations and diversification has not yet been discovered (Bird, 1995).
In the following discussion, I present a hypothesis that seeks to provide an explanation for the seemingly incongruent relationships linking genome duplication events, advancement in organismal complexity and the degree of species diversification in vertebrate evolution. In so doing, I briefly examine current perceptions and problems related to understanding genome and organismal complexity, and provide a simplifying framework for addressing the effects of genome duplication on genetic and organismal complexity that enable a test of the hypothesis.
The genetic value optimum: a possible link between genome and organismal evolution
Despite considerable recent interest in the effects of large-scale genetic duplication on organismal evolution, the current debate is focused almost exclusively on resolution of the 2R hypothesis, which proposes that two rounds of genome duplication occurred early in vertebrate history (Sidow, 1996; Hughes, 1999; Furlong and Holland, 2002). This debate, while useful in attempting to shed light on the evolutionary history of the vertebrate genome, belies a growing consensus, even among critics of the 2R hypothesis, that large-scale genome expansion occurred in vertebrate evolutionary history and that it likely played a central role in vertebrate evolution (Wolfe, 2001). Provided the agreement that large scale genome expansion is a hallmark of vertebrate evolutionary history and that it likely influenced organismal evolution, it seems useful to create a theoretical framework for examining the interrelationships among genome expansion, organismal evolution and species diversification. In an attempt to formulate a theoretical basis for exploring these linkages, I propose the genetic-organism value optimum (GOVO) hypothesis. The primary purpose of this hypothesis is to provide a formal construct for testing the relationship between genome changes, organismal innovation and species diversification.
The GOVO hypothesis posits that there is an intrinsic relationship between genetic value (herein defined as the total functional genome information content) and organismal complexity (herein defined as the sum of the developmental, morphological, and functional complexity of organisms) wherein increases or decreases in either occur in parallel. While this hypothesis is simply a formalization of statements that have been articulated previously in an informal way, it provides a testable framework for evaluation of the linkage between genes, genomes and organisms. There are two major predictions of the GOVO hypothesis: the first is that abrupt changes in genetic value will be matched by similar saltational changes in organismal complexity, and the second is that genetic value should be relatively constant within lineages that demonstrate stable levels of organismal complexity. These predictions of the GOVO hypothesis are most likely to be manifested within the context of large-scale genetic duplications or during extended periods in which organismal complexity within a lineage exhibits stability. A corollary prediction is that abrupt increases in genetic value resulting from genome level duplications that are not paralleled by matching changes in organismal complexity should be followed by a period of declining genetic value culminating in a return of the genetic value to the preduplication level. This prediction infers that large-scale duplications may be inconsequential in the absence of concurrent organismal innovation or species diversification, a likelihood that is only rarely mentioned and not explicitly predicted by existing genome duplication theories (Wolfe, 2001). This line of reasoning also runs contrary to the common presumption that large-scale genetic duplications characteristically parallel a stage of major organismal innovation or accelerated species diversification (Ohno, 1970; Bird, 1995; Holland, 1999).
Based on these predictions, explicit tests of the GOVO hypothesis include determining what happens to genetic value after large-scale genetic duplications both in the presence and absence of concordant increases in organismal complexity. Since testing the GOVO hypothesis requires understanding as well as measuring genetic value and organismal complexity, it is important to discuss contemporary understanding of these issues to define an appropriate system for testing the hypothesis.
Genetic value and organismal complexity
Identification of a system for testing the GOVO hypothesis, necessitates an appropriate approach for measuring, or at least addressing, genetic value and organismal complexity. The scientific literature abounds with an ever more protracted debate about the most acceptable means to measure genetic (genomic) and organismal complexity (Hahn and Wray, 2002; Adami, 2002). However, even the most ardent critics of a relationship between genome duplication and organismal complexity acknowledge that the historical record of evolution provides evidence of a positive correlation between genetic value and organismal complexity (Hughes et al., 2001). The difficulties in refining this relationship then seem rooted largely in reaching a consensus about defining and accurately quantifying genetic value and organismal complexity.
Efforts to define and quantify genetic value have explored related concepts including the historically most prevalent but clearly inadequate metric, the C-value (a measure of genome length). Use of the C-value as a means to estimate functional genetic complexity, i.e., the genetic component responsible for organismal determination, has been cast aside because it has proven impossible to link the vast tracts of the eukaryotic genome composed of simple repetitive elements to organismal function (Zuckerkandl, 2002). More recently, the G-value (the total number of genes in the genome) and the I-value (the number of expressed gene products or even the information content of the genome) have been proposed as more adequate measures of genetic value (Betran and Long, 2002; Weinberger, 2002). The G-value has been criticized as a measure of genetic value in that it fails to take into account the plethora of post-transcriptional and post-translational processes through which genes generate products needed in constructing organisms (Hahn and Wray, 2002). The problem of the g-value might therefore be equated with the inadequacy of existing definitions for the gene. Similarly, the I-value, while conceptually encompassing the expressivity of the genome, is so inclusive and mechanistically ill-defined as to render the concept of little practical utility as a standard of measurement. At issue are problems tied to the vagaries stemming from difficulties in constructing a genotype-phenotype network. A reasonable short-term solution, as is argued in the next section, may be to estimate genetic value within a morphologically and genomically diverse clade in which the systems responsible for gene expression are similar such that the correspondence between genotype and phenotype among the taxa included in the analysis is stable.
A similar dire collection of problems plague estimates of organismal complexity, including how to account for the complexities of intercellular relationships during development, all aspects of organismal function, and hierarchical interactions bridging the entirety of organismal morphospace (Foote, 1993; Kauffman, 1993; McShea, 1996; McShea, 2000; McShea, 2001)
Rather than try to address the myriad substantive but widely debated issues related to measurements of genetic and organismal complexity, I will define a highly simplified system within which it seems feasible to conduct a test of the GOVO hypothesis.
Defining a system to test the GOVO hypothesis
As mentioned, if approached from its broadest dimensions, the measurement of genetic value across living taxa is extremely daunting as it requires comparison of organisms that have evolved vastly different mechanisms for expressing the information content of their genomes. As an example, the nematode, Caenorhabditis elegans, with about a thousand total cells and a very simple tube-like body plan has an estimated 19,000 genes, whereas the fruit fly, Drosophila melanogaster, with an arguably more complex body structure, including a distinctive head, appendages, and a relatively complex brain compared to C. elegans has only 14,000 genes (The C. elegans Sequencing Consortium, 1998; Adams et al., 2000) Despite the apparent discrepancy in gene content, some of which can be accounted for as a result of tandem duplications in C. elegans, D. melanogaster apparently expands the functional utility of its "limited" gene complement by extensive alternative splicing in a fashion unavailable to C. elegans. A more detailed exposition of the problems associated with calculating and comparing the genetic complexity of divergent taxa is provided in several provocative reviews (Szarthmáry et al., 2001; Hahn and Wray, 2002)
A necessary step toward simplification of the genetic complexity problem would be to include only those groups in which gene expression mechanisms are the same or very similar, i.e., in which counting genes or transcripts yields generally equivalent information about genetic complexity in relation to gene number. This approach requires the group to be sufficiently well characterized genetically to justify conclusions regarding the overall equivalence of its genetic expression systems in a background of extensive organismal and genomic level variation. Based on the evidence available from comparative genomics, it is clear some comparisons may be more appropriate than others. In the case of C. elegans and D. melanogaster the differences in structure of "genes" and the resultant generation of splicing products from a single "gene" between the coelomate arthropods and pseudocoelomate nematodes preclude estimates of genetic value based on counting genes. However, comparative genomics suggests that chordates, show a considerable similarity in general mechanisms for gene expression and its control (Coulson and Ouzounis, 2003). An added advantage of this group is the availability of complete genomic sequences for three very divergent members of this group, the human (Homo sapiens), Japanese pufferfish (Takifugu rubripes) and sea squirt (Ciona intestinalis), and a growing body of sequence information for other key taxa including amphioxus (Branchiostoma), sea lamprey (Petromyzon marinus), horned shark (Heterodontus francisi), African clawed frog (Xenopus laevis), zebrafish (Danio rerio) and other mammals and fish species. Given the similarity of gene expression systems among the chordates and a rapidly increasing body of genomic information, there is reason to believe that comparisons of gene numbers among individual taxa could provide meaningful information about their genetic complexity relative to one another.
Although it is tempting to consider deriving estimates of genetic complexity from large-scale genome comparisons, this approach is not yet practical because gene annotation is incomplete even for the most advanced systems (Heilig et al., 2003) However, large-scale genome comparisons have revealed the existence of considerable synteny and the occurrence of extensive paralogons (paralogous chromosome regions) among evolutionarily divergent taxa within the chordates (McLysaght et al., 2002). The occurrence of paralogons in individual members of evolutionarily divergent taxa provides a potential resource for measuring changes in genetic value in relation to large-scale genome duplication events without the complications of annotation that presently plague genome level comparisons. Since paralogons are composed of collections of related genes at different chromosomal locations that arise through the process of gene duplication, it follows that repeated genome duplications create paralogons with an exponentially increasing number of genes. In the absence of gene loss, simple counting of genes within a paralogon can provide a measure of the extent of duplication. Under the assumption that gene numbers relate to genetic value, at least in the cases where gene expression systems are equivalent, counting the number of genes within a paralogon can provide an estimate of genetic value that is intrinsically linked to the evolutionary ancestry of the organisms in which duplications have occurred. While quantifying genetic value through comparison of the number of genes in paralogons does not provide absolute genetic values, it does provide relative genetic values. By counting and comparing the number of expressed genes in paralogons from organisms that represent lineages with divergent genome duplication histories and organismal complexities, it is feasible to assess the relationship between genetic value and organismal complexity and to conduct a test of the GOVO hypothesis.
Measurements of organismal complexity in relation to the genome and evolution are confounded by a host of factors, including definitions of complexity, agreement regarding the organismal constituents that contribute to complexity, as well as the appropriate hierarchical organizational levels to consider (Gould, 1996).
In light of the unresolved nature of these issues, it seems useful to consider certain simplifying assumptions about organismal complexity as a means to identify appropriate qualities to enable a test of the GOVO hypothesis. The most extreme simplification is to consider only the most drastic changes in organismal complexity as relevant landmarks for comparisons. Among multicellular eukaryotes such changes might include the origin of new embryological tissue layers, i.e., the emergence of the diploblastic, triploblastic and neural crest tissue layers and the structures derived from them, whereas within vertebrates it might include the evolution of a complex brain from a simplified cranial ganglion, an endoskeleton, paired appendages, and neurogenic placodes (Shimeld and Holland, 2000). In short, simplification of the complexity issue may best be addressed by adjusting the scale of the complexity measure to encompass only the most deeply rooted or profound innovations, provided there is information on their directionality; which is to say, whether they represent additions to existing structures, rearrangements, or reductive simplifications. By limiting measures of complexity to the most extreme examples, it is relatively straightforward to map the complexity changes in terms of directionality. Also, since the GOVO hypothesis predicts that profound changes in organismal complexity should under most circumstances occur in parallel with similar changes in genetic value, limiting observations to complexity changes characterized by extreme variation provides a favorable background for assessment of the relationship between genetic value and organism complexity.
An initial test of the GOVO hypothesis
The most extensively characterized paralogon within the chordates includes the genes that comprise the Hox gene family (McLysaght et al., 2002). An evolutionarily ancient gene family that encodes transcription factors required for the specification of tissue and cellular identity during embryogenesis, the clustered Hox genes represent a particularly compelling assemblage of genes for use in testing the GOVO hypothesis. The fundamental properties of the Hox genes that recommend them for testing the GOVO hypothesis include their stereotypical clustered organization throughout the vertebrates (Shubert et al., 1993), their extensive characterization within members of the chordate lineage (Amores, 2004), including species that represent divergent lineages with different genome duplication histories (Prince, 2002), including one (Branchiostoma) assumed to be representative of the basal clade within the group (Garcia-Fernandez and Holland, 1994), and their central role in morphological specification of major body axes and structures including appendages. It is also worthwhile noting that the clustered Hox genes do not appear to have undergone intra-cluster tandem duplications, recombination or gene conversion, each of which can confound the analysis of gene duplication history.
The selection of the chordates as an appropriate taxonomic group in which to investigate the relationship between genetic value and organismal complexity has been detailed earlier. To summarize, chordates utilize similar gene expression systems, which increases the likelihood that counting genes in divergent lineages provides similar information about genetic value; they exhibit considerable evolutionary divergence and marked organismal innovation, indicative of large-scale shifts in organismal complexity and useful for the simplified analytical paradigm developed for an initial test of the GOVO hypothesis; their Hox cluster paralogons, which serve as a genome proxy, are extensively characterized and therefore provides suitable genomic information for comparative purposes.
An especially useful property of the Hox cluster paralogon, is the preservation of the order of genes within the paralogon even among the most widely divergent chordates. Although individual clusters differ from one another because of gene loss following cluster duplication, a comparison of clusters within and among species provides strong evidence to infer that the ancestral condition in chordates is a string of 14 tightly linked genes (Powers and Amemiya, 2004). The remarkable feature of this organization is that the inferred composition of the ancestral cluster and the actual composition of the cluster in the extant representative of the presumed prototypical vertebrate ancestor are for all intents and purposes identical. In the context of the GOVO hypothesis, this result is taken to indicate that Branchiostoma can serve as the GOVO genetic value index against which descendent lineages can be compared. Further support for the use of Branchiostoma as an index relates to its relative organismal simplicity in comparison to vertebrates. Despite considerable effort, it has been impossible to identify a tissue in Branchiostoma that corresponds to the neural crest of vertebrates (Escriva et al., 2002). Moreover, Branchiostoma is missing a host of structures considered to be vertebrate innovations, including an elaborate segmented brain, an endoskeleton, neurogenic placodes and all the structures derived from neural crest tissue (Shimeld and Holland, 2000). In this sense, Branchiostoma serves as an ideal index for chordate organismal complexity as it clearly lacks a collection of deeply rooted vertebrate innovations, the most profound of which is the absence of neural crest tissue.
Genetic value and organism complexity comparisons: a further test of the GOVO hypothesis
Under the assumption that the single Branchiostoma Hox cluster is representative of the chordate ancestor of vertebrates and that cluster duplication events occurred by repeated trans duplications (a proxy for genome duplications), it is possible to predict the expected gene value for the various descendent vertebrate lineages under the assumption that the full complement of genes are retained after each duplication event. Table 1 shows the results of a comparison wherein the predicted value for the basal gnathostome is derived from the number of genes resulting from two complete duplications of the 14 gene ancestral cluster, while the observed value is inferred from a composite of the Hox cluster genes documented in extant actinopterygians and sarcopterygians (Amores et al., 1998, 2004; Stellwag, 1999; Meyer and Málaga-Trillo, 1999). Since the sarcopterygian lineage appears to have a stable four clusters with no indication of any additional clusters, their predicted gene value is the same as that for basal gnathostomes, whereas the observed value of 39 is derived from extant mammals and based on exhaustive sequence searches. The predicted value of 112 for actinopterygians is derived from the number of genes that would have resulted from three complete duplications of the 14 gene ancestral cluster based on the observation of an additional complete set of duplicated clusters in extant members of this lineage relative to the stem lineage of gnathostomes (Prince, 2002). The observed value of 47–52 for actinopterygians is taken from the actual number of genes documented after an extensive characterization of the Hox gene complement of zebrafish, Japanese pufferfish and the Southern pufferfish, respectively (Amores et al., 1998, 2004).
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Comparisons of the gene values among these taxa reveal some intriguing relationships. Firstly, the predicted and observed values for basal gnathostomes and mammals are very similar, differing by only three genes out of a predicted maximum of 52 genes. This result suggests that the mammals, and presumably other tetrapods, exhibit a relatively stable Hox gene value with respect to their gnathostome ancestor, with a nearly negligible net gene value loss within the vertebrate lineage leading from ancestral gnathostomes to mammals. While it would be presumptuous to assume that the net gene loss leading from ancestral gnathostomes to mammals is significant, this result underscores the evident stability of gene value extending from ancestral gnathostomes to mammals. An additional observation is that the sarcopterygian lineage has retained a substantial 70% of the predicted gene value relative to its chordate ancestor, which can be interpreted to mean that the gene value optima from chordates through gnathostomes to mammals is quite conserved and indicative of a relatively "efficient" utilization of the expressed genome. This interpretation is dependent on the assumption that organismal complexity remained relative constant between basal gnathostomes and the most complex tetrapods and that the major complexity changes occurred prior to the inception of gnathostomes. In support of this interpretation is the fact that the major vertebrate innovations including the evolution of neural crest, the beginnings of an elaborate segmented brain, an endoskeleton, and neurogenic placodes actually occurred between the inception of vertebrates and the basal gnathostomes (Shimeld and Holland, 2000
). Accordingly, it is consistent to conclude that the level of organismal complexity exhibited by basal gnathostomes could be similar to that of the most advanced members of the sarcopterygian lineage. Alternatively, if the organismal complexity of the most advanced tetrapods is significantly greater than that of basal gnathostomes, it would invalidate the GOVO hypothesis, indicative of the absence of an identifiable linkage between gene value and organismal complexity.
What then of the comparisons between the gene values of the sarcopterygian and actinopterygian lineages? Assuming that a genome duplication event occurred in the actinopterygian stem lineage after the divergence of bichir (Chiu et al., 2004), the predicted number of Hox genes under maximal conditions should be 112 (Table 1). However, the observed number in zebrafish, Japanese pufferfish, the smooth pufferfish and likely in related teleosts, ranges between 48 and 52, which is less than one-half the predicted number and very nearly the same as the inferred value for basal gnathostomes. This result shows that the gene values for basal gnathostomes are similar to those for the sarcopterygian and actinopterygian lineages.
Calculation of the ratio of observed to predicted gene values for the various lineages (Table 1), provides a number that hovers around 0.7 for all the lineages with the exception of the actinopterygians, which dips below 0.5. This dip in the ratio of observed to predicted gene values is indicative of extensive gene loss in the actinopterygians relative to the sarcopterygians, but is based on the assumption of a sharp rise in gene value corresponding to large-scale genome expansion due to a genome level duplication in early actinopterygian evolution. Again, provided that organismal complexity of these two divergent lineages is similar, the GOVO hypothesis predicts an excessive loss of gene value post-duplication in actinopterygians relative to the sarcopterygian lineage in which a parallel genome duplication did not occur. While it is difficult to make definitive statements about differences in organismal complexity in comparisons between the actinopterygians and sarcopterygian lineages, it is certain that the degree of complexity difference is far less than that between ancestral chordates and basal gnathostomes and may even be negligible. If this interpretation is correct, there is reason to suspect that the GOVO hypothesis provides a useful perspective for understanding the relationship between genome and organismal complexity.
Gene value and species diversity
A central question posed at the outset was whether large-scale genome changes, such as occur during polyploidization, likely precede or parallel advancements in organism complexity, promote species diversification, or do both or neither? Based on the forgoing discussion, a case can be made that large-scale genome changes occur concurrently with advancements in organismal complexity but also in their absence. When the genome changes occur in the absence of parallel changes in organismal complexity it appears that gene value is lost concordantly. Is it possible that some of the genome "potential" resulting from genome duplications is devoted to species diversification, thereby leading to the equivalent of a distributed form of organismal complexity (Eble, 2003)? The answer to this question requires information about the rate and extent of speciation in divergent lineages with similar level of organismal complexity but different histories of genome expansion, a condition which it has been argued here exists between the actinopterygian and sarcopterygian lineages.
Based on estimates, the number of extant species derived from the sarcopterygian lineage is approximately 21,000–22,000 compared to about 23–25,000 for actinopterygians (Carroll, 1988; Nelson, 1994). When viewed from the perspective of total numbers, the differences appear rather small, suggesting that the genomic duplication within the stem lineage of actinopterygians would not be required to support such minor differences in species number. However, evidence presented in a recent review by Taylor et al. (2001) indicates that polyploidized members of the families Salmonidae and the Catostomidae, exhibit higher degrees of speciation than members of the same family that remain diploid (Nelson, 1994). As proposed by Lynch and colleagues (Lynch and Conery, 2000; Lynch and Force, 2000) this as an example of "divergent resolution," wherein the differential post-duplication loss of genes creates an effective mechanism for population isolation that promotes speciation. Their interpretation provides a mechanistic explanation consistent with the GOVO hypothesis, which predicts that gene value will decline following large-scale duplication events in the absence of concurrent advancement in organism complexity. While it is difficult to reconcile the different interpretations of the effects of genome level duplications in the example of the actinopteryian stem lineage duplication compared to the salmonid or catostomid duplications, it remains a distinct possibility that genome level duplications are linked to species diversification.
If we accept that large-scale genetic duplications are a hallmark of vertebrate evolution (Shimeld and Holland, 2000) and that vertebrates have a rich history of evolutionary innovation and speciation, it would be consistent to conclude that genome duplications provided a springboard to loft chordates into a trajectory leading to the evolution of novelty, increased organismal complexity, and extensive species diversification. However, it is worth reiterating that the GOVO hypothesis predicts that the evolutionary trajectory of novelty, complexity and diversity linked to genome duplication may be diminished or thwarted entirely by organismal constraints.
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FOOTNOTES |
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1 From the Symposium Patterns and Processes in the Evolution of Fishes presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Canada.
2 E-mail: stellwage{at}mail.ecu.edu
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