Journal of Heredity Advance Access published online on October 22, 2007
Journal of Heredity, doi:10.1093/jhered/esm088
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Significant Variation for Fitness Impacts of ETS Loci in Hybrids between Populations of Tigriopus californicus
From the Department of Biology, University of North Carolina, CB#3280 Coker Hall, Chapel Hill, NC 27599-3280
Address correspondence to C. S. Willett to the address above, or e-mail: willett4{at}email.unc.edu
The connections between the genes that cause hybrid incompatibilities and the physiological processes disrupted in hybrids by these incompatibilities are not well understood. The interactions between proteins in the electron transport system (ETS) in the copepod, Tigriopus californicus, have emerged as a potential model system to explore such connections. In this study, the effects on hybrid fitness of 3 different nuclear loci encoding proteins of the ETS are examined in hybrid copepods obtained from crosses of genetically divergent populations of this species. The potential interactions between these genes and mitochondrial-encoded proteins of the ETS are also explored; these interactions have been shown to have diverged functionally between these populations in other studies. Large deviations from Mendelian inheritance are found in genotypic ratios at each of the 3 loci in adults but not in nauplii, demonstrating genotype-based selection during development. The length of developmental time of hybrids appears to influence the pattern of deviations in these loci, likely in conjunction with levels of competition in these crosses. The major finding of this study is that in repeated crosses, the nature of deviations at these ETS loci shows dramatic differences suggesting that slight perturbations in initial conditions can dramatically shift the patterns of selection at these ETS loci in interpopulation hybrids.
The intertidal copepod species, Tigriopus californicus, provides unique advantages for the study of the coevolution of mitochondrial DNA (mtDNA)–encoded and nuclear-encoded proteins in the electron transport system (ETS). Each of the ETS complexes consists of many subunits in higher eukaryotes, with most complexes containing proteins encoded both by mtDNA and nuclear genes. Intimate interactions between mtDNA-encoded and nuclear-encoded proteins are thus required for the proper functioning of the ETS. Previous studies (summarized in Burton et al. 2006) have shown that the nature of the interactions between these ETS complex subunits has diverged between genetically divergent populations of T. californicus (which have especially large divergences in mtDNA-encoded genes). The evolution of mitochondrial/nuclear coadaptation between populations has been most convincingly demonstrated at a functional level; determination of the impacts on hybrid fitness has yielded sometimes contradictory results. In this study, I will examine the fitness impacts of genotypes at 3 loci involved in the ETS using repeated crosses to help determine the connections between ETS protein functional coadaptation and hybrid fitness.
The fitness of copepods is lower in hybrids resulting from crosses of genetically isolated T. californicus populations along the Pacific coastline of North America. Tigriopus californicus inhabits upper-intertidal rocky pools, a habitat that is often patchy in distribution, with large regions of sandy beach separating rocky outcrops. These sandy regions form a barrier to copepod dispersal resulting in stable genetic differentiation between outcrops (Burton 1997). Divergences in mtDNA between some California populations can exceed 20% (Burton 1998; Edmands 2001; Willett and Burton 2004; Rawson and Burton 2006). Copepods from these populations can be crossed in the laboratory in order to examine the fitness of the hybrids. For a number of different fitness measures the F2 generation (but not the F1 generation) has lowered fitness in comparison to the parental populations, a pattern referred to as hybrid breakdown (Burton 1987, 1990; Edmands 1999; Edmands and Deimler 2004). Postzygotic reproductive isolation of this type is likely to be caused by deleterious interactions between homozygous, recessive incompatibility alleles at one locus with alternate parental alleles from at least one other locus (potentially a mtDNA-encoded locus), a type of Dobzhansky–Muller model hybrid incompatibility (Dobzhansky 1936; Muller 1942; Coyne and Orr 2004). A small handful of the loci that underlie postzygotic reproductive isolation in hybrids between species have been identified (mostly in Drosophila), but the connections to the physiological processes that are disrupted in the hybrids are largely unknown (Wittbrodt et al. 1989; Ting el al. 1998; Barbash et al. 2003; Presgraves et al. 2003; Brideau et al. 2006; Masly et al. 2006). Although most of these genes have been shown to be subject to natural selection, it is largely not clear why this selection has occurred.
In T. californicus, the closely interacting proteins of the ETS form a candidate system in which to study the evolution of hybrid incompatibilities. Although the major portion of the nucleotide divergence in mtDNA genes between copepod populations is silent, there is substantial amino acid differentiation as well, and this amino acid differentiation has led to divergence in the interactions between mtDNA-encoded and nuclear-encoded proteins of the ETS. For complex IV of the ETS, divergence in functional coadaptation of cytochrome c (CYC) and the largely mtDNA-encoded complex IV (the 3 largest subunits of complex IV are mtDNA encoded) has been demonstrated by in vitro assays of enzyme activities between 2 T. californicus populations (Rawson and Burton 2002; Harrison and Burton 2006). Ellison and Burton (2006) found that the enzymatic rates of each of the ETS complexes were negatively impacted in hybrids between a set of copepod populations, with the notable exception of complex II, which does not contain any mtDNA-encoded subunits. They also found a correlation between the amount of adenosine triphosphate produced by mitochondria and survivorship in these hybrids, implying a link between mitochondrial performance and fitness.
The relative viability of genotypes at several ETS-associated genes in hybrid copepods has been studied by examining deviations from expected Mendelian patterns of inheritance in F2 and advanced generation hybrids. With the maternal inheritance of mtDNA in this species, by performing reciprocal crosses, the effect of mtDNA (coupled with cytoplasmic background) on the viabilities of ETS-associated genes can be determined. Willett and Burton (2001) found that there was not a universally positive effect of matching the cytoplasmic and CYC genotype in hybrids of crosses between 3 different copepod populations, but there were substantial differences between reciprocal crosses suggesting cytoplasmic effects. In one specific cross (Abalone Cove [AB] males crossed to Santa Cruz [SC] females), deviations were consistent with mitochondrial/nuclear coadaptation in repeated crosses and advanced generation hybrids under 2 of 3 different temperature and light regimes (Willett and Burton 2003). Willett (2006) looked at the relative viabilities of 2 nuclear-encoded genes that are integral parts of complex III of the ETS (rieske iron–sulfur protein [RISP] and cytochrome c1 [CYC1]) in addition to CYC (CYC is a soluble protein that interacts with both complex III and complex IV of the ETS) in hybrids from crosses of 2 copepod populations, San Diego (SD) and AB. For these 3 genes, again there was not a consistent positive association of genotype with mtDNA background, but there was significant epistasis between each of the 3 genes suggesting that nuclear/nuclear coadaptation in complex III has diverged between these 2 populations. Notably, the F2 nauplii (the first larval copepod stage) did not show deviations from expected Mendelian patterns of inheritance in these crosses, implying that the selection is occurring during the course of development.
These studies of the effects of ETS loci on hybrid viability suggest that differences in enzymatic rates and mitochondrial function may not translate in a simple way to hybrid viability. For example, functional coadaptation was found between CYC and complex IV between the SD and SC populations (Rawson and Burton 2002; Harrison and Burton 2006), but coadaptation was not evident in the genotypic viability data for this cross (Willett and Burton 2001). Environmental conditions (temperature in particular) appear to play a large role in influencing the outcomes of both functional and fitness assays and may contribute to this discrepancy (Rawson and Burton 2002; Willett and Burton 2003; Harrison and Burton 2006). However, even under similar environmental conditions, in a few cases divergent results have been found for the viability of ETS loci (Willett and Burton 2001; Willett 2006). Here I will further explore the degree of repeatability of deviations from expected patterns of inheritance for these ETS loci in F2 hybrids of interpopulation crosses. I will also examine the link between developmental time and selection at these ETS loci. In some cases, there are substantial differences between repeated crosses suggesting that slight differences in conditions can dramatically influence the impact of these ETS loci on the fitness of hybrid copepods.
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Copepod Collection and Culturing
Tigriopus californicus were collected from intertidal rock pools at 2 sites in southern California, SD (32°44.74'N, 117°15.30'W, San Diego County) and AB (33°44.26'N, 118°22.52'W, Los Angeles County), and one site in central California, SC (36°56.97'N, 122°02.82'W, Santa Cruz County). There are large genetic divergences between these populations, with about 20% divergence between each population in cytochrome b sequences (mtDNA encoded), whereas divergence in the coding regions of 9 nuclear-encoded genes averages 1.5% (Willett and Burton 2004; Willett and Berkowitz 2007). Within a single population, levels of genetic polymorphism are much lower, with an average of 0.3% divergence between any 2 sequences from one site for the same set of nuclear and mtDNA genes. After collection, the copepods were maintained in mass culture in artificial seawater (Instant Ocean, Aquarium Systems Inc., Mentor, OH) in 400-ml beakers at 20 °C with a 12:12 light:dark photoperiod. Cultures were maintained at concentration of 35 parts per thousand seawater and fed with commercial flake fish food, but copepods were also allowed to consume natural algal growth.
Population Crosses and Hybrid Collection
To test the nature of potential viability differences resulting from proteins involved in complex III of the ETS in F2 hybrids, I set up crosses using copepods from different populations that had been maintained in the culturing conditions described above for at least 1 year (multiple generations are likely to have occurred in these laboratory conditions). Crosses were done between the AB and SC populations and the SC and SD populations using 20–25 males and the same number of virgin females in each of at least 2 petri dishes per cross. F1 hybrids progeny from these crosses were allowed to intermate (F1 dishes were mixed to help prevent inbreeding), and then mated F1 females were transferred to new plates (
25 per plate) in which they produced F2 hybrids. F1 females were transferred to new dishes on the appearance of F2 copepodids to ensure that generations were kept separated. The effect of using at least 40 individuals from a population to initiate crosses will be to average over the genetic variation within each population. Both reciprocal crosses were made for the SC/SD and AB/SC populations. Another complete set of crosses were made for the AB/SC populations (set 2) after the completion of the first set (set 1), whereas only a single set of crosses was done for SC/SD.
F2 copepods were collected as both nauplii and adults and DNA prepared from F2 individuals by the methods described in Willett (2006). Two 96-well plates of F2 nauplii were collected from a single set of reciprocal crosses for the SD/SC and AB/SC populations. For set 1 from the AB x SC cross, two 96-well plates each of males and females were collected (4 total adult plates from each reciprocal cross). Five plates of combined male and female F2 adults were collected from each of the 2 SD x SC crosses and the ABf x SCm set 2 cross, whereas 7 plates were collected for the ABm x SCf set 2 cross. All copepods developing to the adult stage were collected from 2 of 3 dishes from the ABm x SCf set 2 cross, whereas all other dishes in the other crosses were not exhaustively sampled. For adults collected from the SC/SD and AB/SC set 2 crosses, an estimate was made of developmental time by noting the number of days from when F1 females were removed from plates that it took for the F2 hybrids to complete development. This is an imprecise measure of development time because there is variation in the age of F2 offspring in a dish when the F1 females are removed.
Genotyping ETS Loci and Statistical Analyses
The F2 copepods from these crosses were genotyped for 3 different loci involved in complex III of the ETS, RISP, CYC1, and CYC, using a polymerase chain reaction (PCR) assay that generated diagnostic, population-specific alleles lengths for codominant scoring of genotypes (primer sequences and PCR conditions available from C.S.W. on request; see also Willett and Burton 2001; Willett 2006). The F2 hybrids were tested for departures from homogeneity between sexes and for differences between petri dishes in the ABm x SCf cross using contingency tests at each of the 3 ETS markers. Deviations from Mendelian 1:2:1 ratios were examined for the sexes separately and for the combined sample with a 
2 analysis. The potential role of developmental time was examined by breaking the total sample from each cross in half by date and testing whether there were significant differences between the fast-developing and the slow-developing hybrid copepods with contingency table analysis. The relative viabilities of homozygous genotypes (assuming the heterozygote has a viability of one) and their standard deviations were calculated according to Haldane's (1956) formulae.
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AB and SC Hybrids and ETS Viabilities
Two sets of both reciprocal crosses were initiated at different times between the AB and SC populations of T. californicus, and hybrid F2 nauplii and adults were genotyped for 3 complex III–associated markers for each of these crosses. In many of these crosses for F2 adults but not nauplii, there are significant departures from expected 1:2:1 Mendelian patterns of inheritance and differences between male and female hybrids for the ratios of genotypic classes at CYC, RISP, and CYC1 (Table 1 and Supplementary Table S1). For CYC (Figure 1), the patterns of deviations at these 3 genes are not consistent across the 2 sets of crosses in this study, nor when compared with analogous crosses from Willett and Burton (2001). For the SCf x ABm set 2 cross, we can further break the results down by the offspring produced from 3 different replicate dishes of F1 females (Table 2). For CYC, there was only one dish (3) that showed a skewed genotypic ratio (and was significantly different from the other 2), whereas for CYC1 2 dishes showed skewed genotypic ratios (and were different from dish 1). In Figure 2, we can see that CYC1 generally shows a deficit of AB/AB homozygotes across all crosses, and the same pattern is seen for 2 of 3 dishes in set 2 (Table 2). RISP only shows significant departures from Mendelian inheritance for the set 2 ABf x SCm cross (Figure 3). Finally for the AB/SC set 2 crosses, developmental time had a significant effect (P
0.04) on genotype for 2 marker/cross combinations; in the ABf x SCm cross, CYC had more extreme bias from expected Mendelian patterns in faster developing copepods, and CYC1 in the same cross had more bias in slower developing copepods (Supplementary Table S2).
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SD and SC Hybrids and ETS Viabilities
For the crosses between the SD and SC populations, there are again large departures from Mendelian inheritance and significant differences between males and females in F2 adults but not in F2 nauplii for RISP, CYC, and CYC1 genotypic ratios (Table 3 and Supplementary Table S3). Only one set of crosses was done for these 2 populations, but for CYC in Figure 4, we can compare the results from this set to those performed under nearly identical conditions previously (Willett and Burton 2001). In the SDm x SCf cross, there are large differences between the 2 sets of crosses in genotypic ratios for CYC with the opposite homozygous class underrepresented in each. The CYC1 and RISP (Figure 5) markers show substantial differences between reciprocal crosses, but these markers were not included in the previous study, so comparisons across SD x SC crosses cannot be done for these 2 markers. Of the 6 marker/cross combinations for SC/SD in this study, 4 have significant effects of development time on genotypic ratios (Supplementary Table S2). In one of these, the faster developing copepods are more biased (in the SDm x SCf cross for CYC, with the significance of difference genotypic ratios between fast and slow developmental times being P = 0.016). The other 3 are more biased in the slower developing copepods (in the SDf x SCm cross CYC1 [P = 0.003] and RISP [P = 0.03] showed this direction of bias as did RISP in the SDm x SCf cross [P = 0.015]). For both AB/SC and SC/SD crosses, there were no significant 2-way interactions between the RISP, CYC1, and CYC genes (data not shown).
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The RISP, CYC1, and CYC genes that code for proteins associated with complex III of the ETS show significant skews from Mendelian ratios of inheritance in F2 hybrids of population crosses of T. californicus. This skew is found in the adults but not in the first-stage nauplii, implying that selection is acting during the course of development. In a separate study (Willett and Berkowitz 2007), 2 other markers in malic enzyme homologs showed dramatic departures from Mendelian inheritance in the adults but not nauplii, suggesting that this pattern of selection during development may not be uncommon in these hybrid copepods. These skewed genotypic ratios are likely to result from deleterious interactions between genes in the regions of these markers with other loci, as opposed to meiotic drive or other forms of gametic selection. Very few other studies have shown that deviations from Mendelian inheritance in hybrids are due to differential mortality during development (Rogers and Bernatchez 2006 find this for a number of loci in hybrids of whitefish ecotypes). In contrast to the results of Willett (2006), who found evidence for nuclear/nuclear gene interactions between these 3 ETS nuclear-encoded genes in AB x SD crosses, there was no evidence of significant interactions between the 3 ETS genes in the crosses examined in this study.
Of the 3 ETS genes used in this study, CYC has been the best studied previously in T. californicus both from a functional standpoint (particularly its interactions with complex IV) and from a fitness standpoint (by examination of genotypic viabilities for this locus in hybrid copepods). Functional coadaptation between CYC and complex IV was found in comparisons of the SD and SC populations (Rawson and Burton 2002), and this coadaptation was subsequently parsed into the individual effects of each of the 3 amino acid differences in CYC between these 2 populations (Harrison and Burton 2006). In contrast to the results found in these functional studies, there is not consistent evidence for mitochondrial/nuclear coadaptation in the studies of genotypic viability for CYC in crosses between SD and SC (Figure 4). With mitochondrial/nuclear coadaptation, the expectation is that the homozygote class matching the mtDNA type in a cross would have higher fitness than the alternate homozygote class. For SD x SC, this pattern is only seen in F2 females from the SDm x SCf cross in the new cross where the SC/SC homozygote class has 2-fold higher viability than the SD/SD homozygote class (but note the similar pattern found in the reciprocal cross and the opposite pattern found in the 2001 data). These results suggest that either CYC and its interactions with mitochondrial-encoded subunits are not a significant force in shaping viability in F2 individuals in the SC/SD cross (and effects found at these loci are caused by interactions of linked genes) or that slight variations in conditions will impact the nature of the mitochondrial/nuclear coadaptation and its effect on viability.
In crosses between the AB and SC populations, it does appear that slight variations in conditions can dramatically shift the pattern of genotypic viabilities for CYC in F2 hybrids of these 2 populations (Figure 1). In the 3 sets of ABf x SCm crosses, all performed at a constant 20 °C, there are different patterns in each: male AB/AB homozygotes had lower viability in 2001, female AB/AB had higher viability in set 1, and female AB/AB had lower viability in set 2. Note that these differences in results are not likely to result from false positives given the magnitude of the deviations and the large sample sizes of F2 adults (Table 1). It is also unlikely that the differences result from differential sampling of genetic variation within each population for 2 reasons: first, a large number of copepods were used from each population to set up both generations of the cross which should have the effect of averaging out across intrapopulation genetic variation. Second, the magnitude of genetic variation is much lower within each of these populations than between the populations (Willett and Burton 2004). In the reciprocal cross, there is a general pattern of higher fitness for the SC/SC class in comparison to the AB/AB class but a great deal of variation in the magnitude of this effect. In this ABm x SCf cross, previous studies have shown results consistent with mitochondrial/nuclear coadaptation, namely, that the SC/SC homozygote class has higher viability than the AB/AB homozygote class in F2 adults. In addition to the 2001 results included in Figure 1, another cross was performed at 16 °C by Willett and Burton (2001) that showed higher SC/SC CYC viability, and subsequently, advanced generation hybrids from this cross continued to show this pattern of higher SC/SC viability (Willett and Burton 2003). Interestingly, in a second cross performed under slightly different conditions (cycling between 16 and 25 °C daily), there was no evidence for selection for SC/SC homozygotes in the F2 or in advanced generation hybrids. In crosses between the AB/SD populations, some variation between crosses was also seen although the markers that could be compared were more limited (Willett 2006). For CYC genotypic viability from 2 replicates of the same ABf x SDm cross, there were substantial differences in the genotypic viabilities in the F2, despite both being performed under similar conditions.
The widely varying results found for CYC and CYC1 in replicate F1 female dishes within a single set of crosses for ABm x SCf (Table 2) illustrates most clearly how slight variations can yield dramatically different patterns of viability at these ETS loci. These dishes were set up using a mix of F1 hybrids produced by the same set of parents. Although the same number of fertilized F1 females were started in each dish (and levels of food were equal), there were differences in the number of F2 nauplii produced and eventually F2 adults between plates. For these 3 dishes, the order of F2 offspring density was 2 >> 1 > 3 (Willett C, personal observation), having different numbers of copepods in these dishes could influence the levels of competition and alter the relative survival of hybrid copepods. No clear pattern emerges from a comparison of the deviations at CYC and CYC1 and the density in these 3 dishes in this cross. Dish 1 showed little skew in genotypic ratios for either marker, whereas dish 3 was skewed for both, and dish 2 was skewed only for CYC1. Another potential source of variation between these plates is the amount of natural algae growth between plates (under the culturing conditions used, the artificial salt water starts out with no algae, but algae subsequently begins to grow, possibly being transferred in the copepod gut from one dish to another). Genetic variation within a population could be another source of variation contributing to differences between crosses, but this would seem unlikely particularly for this cross where F1 hybrids were taken from the same sets of parents. Although no clear patterns emerge from the exploration of these factors in this study, future experiments could help determine if differences in the degree of competition within a dish manipulated by such factors as copepod and resource density will mediate the nature of deviations found at these ETS genes.
Developmental time is one of the measures of hybrid fitness that is negatively impacted in F2 hybrids in population crosses of this copepod (Burton 1987, 1990) and may be related to patterns of selection at these ETS loci. A simple expectation for the relationship between developmental time and genotypic viability would be that higher fitness genotypic combinations would develop more rapidly than less fit combinations (which could differentially bias genotypes for either the faster or the slower developing classes of hybrid offspring depending on the nature of deleterious interactions and the magnitude of their effects). With the somewhat crude measure of developmental time used in this study, in about half of the marker/cross combinations, there is a significant effect of developmental time on the ratios of genotypes obtained in F2 adult hybrids; however, there is not a consistent pattern of faster or slower developing copepods having greater skew (in 4 of these 6 significant cases, the slower developing copepods had greater skew). Clearly, there is an interaction between developmental time and genotypes at these 3 ETS genes (most pronounced for first-stage nauplii, which do not show skews from Mendelian inheritance). Further studies are needed to help clarify the nature of these interactions between genotypes and the speed of development of F2 hybrids in these crosses, in addition to any potential connections to levels of competition between developing copepods.
Another factor to consider in this study is that the ETS genes themselves may not be causing the departures from Mendelian expectations that I have found in F2 adults; it is possible that linked genes are actually involved in the interactions. For CYC1 in the AB x SC cross (Figure 2), the consistent results across reciprocal crosses suggest that the CYC1 protein may not itself be involved in deleterious interactions in this particular cross, with at least many of the most obvious potential partners. First, the lack of an effect of cytoplasm suggests a significant interaction with mtDNA is not occurring, and second, the lack of interactions with CYC and RISP (interactions that were found in AB x SD hybrids by Willett 2006) suggest that these closely interacting proteins are not partners in substantial deleterious interactions. There may be other potential partners for CYC1 in this particular cross, but it could be more likely that a linked gene is actually leading to the observed departures in genotypic ratios in the hybrids for this cross. Given the long periods of independent evolution between these copepod populations, it would not be surprising if CYC1 were involved in a deleterious interaction in a cross with one population (e.g., AB x SD) but not with another (e.g., AB x SC) depending on the different genetic changes that have accumulated in each lineage.
The results of this study coupled with past work on the effects of mitochondrial/nuclear coadaptation on fitness in interpopulation crosses of T. californicus suggest that functional differences in the ETS may translate in a complex fashion to fitness. Minor changes in the environment appear to significantly alter the impact of ETS loci on hybrid fitness. This result could be more common than generally appreciated in postzygotic reproductive isolation, particularly for crosses between populations or species that have recently diverged. Temperature in particular has been found to influence the expression of postzygotic reproductive isolation in crosses between genetically differentiated populations or species (Wade et al. 1999; Bordenstein and Drapeau 2001; Edmands and Deimler 2004; Demuth and Wade 2007a, 2007b) or alter the effects of loci or genomic regions involved in postzygotic reproductive isolation (Coyne et al. 1998; Barbash et al. 2000; Willett and Burton 2003). Many of the overall genetic changes between recently diverged species that might have accumulated by selection (and could secondarily result in hybrid incompatibilities via Dobzhansky–Muller style interactions) may be more likely to be the result of fine-tuning to differences in either the external environment (e.g., local adaptation) or the internal environment (e.g., compensation for previously fixed deleterious mutations). If this is the case, we might expect to see sensitivity to environmental variations like those that are likely to have generated the variability across replicates found in this study.
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Supplementary tables S1–S3 can be found at http://www.jhered.oxfordjournals.org/.
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National Science Foundation (DEB-0516139).
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I would like to thank Q. Qin, E. Hoddeson, E. Washburn, J. Berkowitz, and H. Leisy for help with copepod crosses and collection and M. Servedio and C. Ellison for helpful comments on an earlier draft of the manuscript.
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Corresponding Editor: John Burke
Received May 10, 2007
Accepted September 17, 2007
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