*Museum of Natural Science
and
School of Forestry, Wildlife, and Fisheries, Louisiana State University at Baton Rouge
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Abstract |
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Introduction |
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These analyses of lineage-based rates and partition divergence patterns assume that DNA hybridization measures mainly scnDNA differences among species, with the bulk of repetitive DNA having been removed and the influence of mtDNA overwhelmed by the much larger nuclear genome. Thus, a DNA-DNA hybridization distance theoretically reflects an average of a wide range of scnDNA divergences between two species and not that of a small, perhaps aberrantly evolving, portion of the nuclear genome or mtDNA. As best we can tell from analyses of the DNA hybridization technique (e.g., Britten, Graham, and Neufeld 1974
), congruence among phylogenetic trees (e.g., Bledsoe and Raikow 1990
; Sheldon, Whittingham, and Winkler 1999
), and the behavior of DNA hybridization in a phylogenetic context or under perturbation (e.g., Bleiweiss and Kirsch 1992
; Sheldon and Kinnarney 1993
), this assumption is valid.
In this paper, we use uncorrected heron scnDNA hybridization distances to assess patterns and rates of heron mitochondrial cytochrome b gene sequence evolution. The nuclear and mitochondrial DNA data were compared in two ways, as discussed above. First, cytochrome b sequences were subdivided by codon and protein region positions into as many as 18 partitions. Genetic distances between pairs of species then were computed from these partitions and plotted against DNA hybridization distances to permit a graphical comparison of divergence patterns. Second, we examined lineage-based rates of molecular evolution. These comparisons were possible because the two data sets yielded congruent estimates of heron phylogeny. Phenetic and patristic (branch length) distances in both data sets were examined via relative-rate tests (Sarich and Wilson 1967
), and the correlation of lineage-based rates between the cytochrome b and DNA hybridization trees was tested by the method of Omland (1994, 1997
).
The comparison of scnDNA hybridization and cytochrome b sequence data also provided a taxonomic congruence assessment of heron phylogeny. Until now, there have been only two modern phylogenetic studies of herons: DNA hybridization studies (Sheldon 1987b
; Sheldon and Kinnarney 1993
; and Sheldon, McCracken, and Stuebing 1995
) and a cladistic analysis of osteological characters (Payne and Risley 1976
). These two data sets yielded fundamentally different estimates of heron phylogeny (fig. 1
), but it was unclear which estimate was better. The cytochrome b sequence analysis breaks this log jam and shows via phylogenetic congruence (Bledsoe and Raikow 1990
) that the DNA hybridization tree is probably more accurate than the cladogram derived from osteological characters. The cytochrome b data also help to resolve some relationships that were unclear in the DNA hybridization tree.
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Materials and Methods |
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Cytochrome b Sequencing
To minimize contamination of the mitochondrial cytochrome b sequences with paralogous nuclear pseudogenes (Quinn 1997
), we used relatively mtDNA-rich tissues as sources of DNA, rather than blood samples, which have relatively low mtDNA copy numbers (Sorenson and Fleischer 1996
). We also amplified the entire cytochrome b gene as a single piece, rather than in smaller sections, to help reduce the chance of amplifying nuclear pseudogenes. Possible pseudogene contamination was also checked by partition analysis to see if the sequences exhibited pseudogene properties (stop codons, equal rates in all codon site positions, lack of domain-specific amino acid conservation, etc.).
Genomic DNA was isolated from 0.1 g of heart, liver, or muscle tissue using standard phenol/chloroform extraction (Hillis et al. 1990
). Most of the mitochondrial cytochrome b gene and part of the adjacent threonine tRNA gene (chicken mtDNA genome positions 1499116063; Desjardins and Morais 1990
) were amplified by the polymerase chain reaction (PCR) from total genomic DNA preparations using a combination of bird-specific and heron-specific primers. The gene was amplified as a single continuous fragment using the primer pair L14990 (5'-CCATCCAACATCTCAGCATGATGAAA-3') (Kocher et al. 1989
) and H16064 (5'-GGAGTCTTCAGTCTCTGGTTTACAAGACC-3') (Helm-Bychowski and Cracraft 1993
). Numbers in the primer names refer to the 3' base positions of the primers as referenced to the chicken mtDNA sequence (Desjardins and Morais 1990
). "L" and "H" refer to heavy- and light-strand primers. PCR reactions were carried out in a GeneAmp PCR System 2400 oil-free thermocycler (Perkin Elmer Applied Biosystems, Norwalk, Conn.), using a 50-µl reaction volume containing 0.5 µM of each primer, 10 mM of each dNTPs, 2.5 mM MgCl2, and 1.25 U Taq polymerase (Perkin Elmer). Thermal cycling was as follows: 35 cycles with denaturation at 94°C for 30 s, annealing at 52°C for 30 s, and extension at 72°C for 30 s. These cycles were followed by a final extension at 72°C for 7 min.
PCR products were electrophoresed in 1% agarose gel at 110 V for 1 h, stained with 10 µg/µl ethidium bromide, excised, and purified using GeneClean II (BIO-101, La Jolla, Calif.) and QIAquick Gel Extraction Kits (QIAGEN, Santa Clarita, Calif.). Both strands of the PCR product were sequenced using various combinations of the primers noted above and the following internal primers: (1) L15320 (5'-GGATACGTCCTACCATGAGGACAAATATCCTTCTGAGG-3'), (2) H15425 (5'-GGAGGAAGTGTAAAGCGAAGAATC-3'), (3) H15710 (5'-GTAGGCGAATAGGAAGTATC-3'), and (4) L15656 (5'-AACCTACTAGGAGACCCAGA-3'). We developed the first two primers, and the latter two are from Helm-Bychowski and Cracraft (1993)
. For manual sequencing, we performed chain termination sequencing (Sanger, Nicklen, and Coulson 1977
) with a 70170 Sequenase PCR Product sequencing kit (Amersham/UB, Cleveland, Ohio). Sequencing products were electrophoresed through a 6% polyacrylamide gel and visualized by autoradiography. For automated sequencing, we used a BigDye Terminator Cycle Sequencing Kit (Perkin Elmer Applied Biosystems), followed by sequencing in an ABI 377 automated sequencer (Perkin Elmer Applied Biosystems) with a 5% Long Ranger (FMC) gel. Light- and heavy-strand sequences that were obtained manually were scored visually, whereas those collected from the ABI 377 were scored using Sequencher 3.1 (Gene Codes Corporation, Ann Arbor, Mich.). The newly generated cytochrome b sequences have been deposited in GenBank; accession numbers are listed in table 1
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Data Analysis
The heron cytochrome b sequences were aligned by eye relative to the chicken sequence (Desjardins and Morais 1990
) using editing and translation features in MEGA (Kumar, Tamura, and Nei 1993
). Base frequencies, site variation, transition and transversion values, and some distance values also were determined with MEGA. Parsimony and maximum-likelihood trees were constructed and bootstrap analysis was performed with PAUP*, version 4.0b1 (Swofford 1998
). The appropriate minimum-parameter, maximum-likelihood model was determined by likelihood ratio tests of the sequence data optimized on a neighbor-joining tree via Model Test 2.0 (Posada and Crandall 1998
). The most appropriate model appeared to be the Kimura (1981)
three-parameter model (K3P), with adjustments for unequal nucleotide frequencies and site-specific rate differences (K3Puf + gamma). Distance values used in tree-building were computed by PAUP*, and distance trees were constructed by least-squares using PHYLIP, version 3.5c (Felsenstein 1995
). Alternative tree branching patterns were constructed with MacClade (Maddison and Maddison 1992
).
To partition the cytochrome b sequence data, we followed the logic of Griffiths (1997)
. The data were partitioned as transitions and transversions according to (1) codon position and (2) protein region and codon position. The first division resulted in six partitions (three codon positions x two states [transition or transversion]). The second division resulted in 18 partitions (three codon positions x two states x three protein regions). The protein regions were the matrix, transmembrane, and intermembrane regions as defined by Zhang et al. (1998)
. Each partition of the data was graphed as uncorrected percentage of difference (MEGA's p-distance) versus DNA hybridization distance (uncorrected Tm, as defined by Sheldon and Bledsoe 1989
). To estimate the instantaneous transition : transversion ratio (Ti/Tv), we used three methods. Ti/Tv was measured as the steepest slope of Ti/Tv plotted against DNA hybridization distance, as the steepest slope of transitional distances plotted against transversional distances (Hasegawa, Kishino, and Yano 1985
; Moore and DeFilippis 1997
), and from the maximum-likelihood rate parameters estimated by PAUP*.
Trees were inferred from cytochrome b sequences, without reference to the DNA hybridization data, by the following methods: (1) weighted parsimony, (2) maximum-likelihood using the K3Puf + gamma model (transition rate = 6.082, AC and G
T = 1, A
T and G
C = 0.4858,
= 0.2698), and (3) least-squares fitting of K3Puf and K3Puf + gamma distances. Trees were also inferred using sequence partitions that exhibited the most linear distance-to-"time" relationship when DNA hybridization distances were used to estimate time. Searches for best trees were heuristic and consisted of 100 parsimony or 20 maximum-likelihood randomized efforts with TBR branch-swapping and MULPARS options in effect. Fifty percent majority-rule bootstrap trees were built from 100 pseudoreplicates. The significance of differences in branching patterns between the best DNA hybridization topology and the most parsimonious or maximum-likelihood cytochrome b trees were determined via the Kishino-Hasegawa test (Kishino and Hasegawa 1989
) implemented in PAUP*.
Rates of cytochrome b evolution were examined using a relative-rate test (Sarich and Wilson 1967
) consisting of Friedman repeated-measures ANOVA on ranks, followed by Student-Newman-Keuls pairwise comparisons (Houde 1987
). Distances from each of the seven outgroups to each heron species were compared. We tested phenetic distances (uncorrected proportional distances) and patristic distances (tree length distances) for a variety of data partitions. We used relative-rate tests to determine rate variation, instead of likelihood ratio (e.g., Sorhannus and Van Bell 1999
) or other tree-based tests (e.g., Felsenstein 1984
), because relative-rate tests indicate specifically which lineages differ in rates and by how much they differ.
Lineage-based rates of molecular evolution were compared between cytochrome b and DNA hybridization trees using the total-evolution method of Omland (1997)
. To perform this test, we used the DNA hybridization tree, which was congruent with cytochrome b trees based on bootstrap support, and then (1) optimized the DNA hybridization and cytochrome b distances and characters on this topology by least-squares and maximum-likelihood, respectively; (2) determined the total length of each lineage from heron ingroup node to branch tip (="total evolution"); and (3) computed contrasts (differences) between pairs of total-evolution values as described by Omland (1997)
. To determine whether the contrasts needed to be corrected for a node-density effect, i.e., a bias in which rate of evolution is directly correlated with number of tree nodes (Fitch and Bruschi 1987
), we first plotted total evolution as a function of number of nodes. The final contrasts were either positive or negative in sign. The degree to which contrasts agreed in signs between trees was determined and tested using a nonparametric binomial test, with the null hypothesis that 50% of the signs would agree by chance.
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Results |
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Lineage-Based Rates of Evolution
Comparisons of phenetic and patristic distances from the seven outgroups to all heron species by Friedman repeated-measures ANOVA indicated significant differences in distances between certain heron lineages. However, outgroup-to-ingroup distances differed depending on the type of distance measure. For example, when distance values were corrected using the K3Puf + gamma method, the tiger heron (Tigrisoma) distance was fairly long, the bittern (Botaurus, Ixobrychus, and Zebrilus) distances were not particularly long, and the Egretta distances were short. This pattern is evident in figures 6A and C.
When distance values were derived solely from third-position transversions, the pattern of relative length changed dramatically: the tiger heron and boat-bill distances became significantly shorter than most other heron distances, and the egret and, especially, the bittern distances became longer. This pattern is evident in figure 7A.
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Discussion |
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Unfortunately, because of poor resolution in parts of the cytochrome b and DNA hybridization trees, we are not able to answer some other questions about heron relationships. With the exception of the interrelationship among great blue herons (Ardea herodias), great egrets (Casmerodius albus), and cattle egrets (Bubulcus ibis), the cytochrome b sequence data did not clarify branching positions within clades. Within the large clade consisting of day and night herons, for example, relationships among the main groups remain unclear. It is not even certain whether the night herons are monophyletic. Similarly, at the basal end of the heron tree, it is not clear whether boat-billed (Cochlearius) and tiger herons (Tigrisoma) are sister taxa or consecutive outgroups. The cytochrome b analyses suggest that the tiger heron is the outgroup to the other herons, but this positioning does not hold up particularly well to bootstrapping (61% support; fig. 6D
). DNA hybridization might have solved this problem, except that two DNA hybridization studies yielded different topologies for the lineages deriving at the base of the heron tree. In Sheldon (1987b
), tiger herons and boat-billed heron were supported as sister taxa by jackknife analysis. In Sheldon, McCracken, and Stuebing (1995)
, two more tiger heron species were added to the matrix, and bootstrap analysis supported tiger herons as the outgroup to all other herons, including boat-billed heron. However, in this latter study, only four species were used to represent the other heron clades. Thus, in both of the DNA hybridization studies, taxon sampling was inadequate. To reflect this uncertainty in the DNA hybridization results, we represented the tiger heron and boat-billed heron relationships as a multifurcation (fig. 1A
). Except for the Ardea, Casmerodius, and Bubulcus case mentioned above, the unresolved DNA hybridization tree (fig. 1A
) still represents the best estimate of heron phylogeny, even after the cytochrome b analyses presented here.
The reason for the lack of resolution within the day and night heron clade and at the base of the heron tree is unclear. Resolution may be difficult (or impossible) simply because the unresolved nodes are too closely spaced in time to be teased apart. However, tightly spaced divergence dates may not explain the whole problem; limitations in the two molecular data sets appear to have contributed uncertainty as well. DNA hybridization cannot resolve close branching points in bird trees because of its substantial measurement error (± Tm 0.2 for herons; Sheldon 1987b
) combined with the relatively slow rate of bird scnDNA evolution. Indeed, one reason we repeated the phylogenetic analysis of herons using the cytochrome b gene was to take advantage of that gene's relatively fast rate of evolution and supposed ability to resolve relationships among closely related taxa (Moore and DeFilippis 1997
). However, the evolutionary rate of the cytochrome b gene appears to have been too fast in most cases. Virtually the only cytochrome b data that were resilient to bootstrapping involved divergence values below 11%, i.e., unsaturated data (fig. 2
). This divergence range was limited to species within the Egretta-Syrigma, Ardea-Casmerodius-Bubulcus, and bittern-Zebrilus clades (fig. 6D
). Although we identified partitions of the cytochrome b gene sequence that had the potential to resolve more distant relationships (e.g., third-position transversions), these data appeared to be too few to stand up to bootstrapping when used by themselves or when weighted heavily and used in conjunction with the rest of the sequence data.
Measures of Relative Time
In the absence of absolute divergence dates, DNA hybridization distances were used in graphs to provide a perspective of cytochrome b sequence change over relative time (figs. 25
). Usually, relative time is represented on the x-axis by total (unpartitioned) sequence distances corrected for back mutations (e.g., Hackett 1996
; Griffiths 1997
). That the two approaches to estimating relative timeDNA hybridization distance and corrected total sequence divergenceyield different perspectives on patterns of sequence change is apparent when figure 3A
is compared with figure 8
. Figure 3A
depicts third-position transversional distances plotted against DNA hybridization distances; figure 8 depicts third-position transversional distances plotted against total cytochrome b distances that have been corrected for back mutations by the K3Puf and K3Puf + gamma methods, respectively.
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In comparison with the plots in figure 8
, the DNA hybridization plot (fig. 3A
) displays more linearity and less variance. It also exhibits fairly distinct clusters of points. These clusterse.g., at Tm
12, 2.5, 3.54, 6, and 10reflect primarily distances among species in separate, major clades. The most obvious and consistent set of such distances is between ingroup and outgroup members (herons to ibis,
Tm ~ 10). In figure 8 , clusters of distances are evident only between ingroup and outgroup members and among the least diverged taxa. Other clusters are obscured by either compression of distances (K3Puf plot) or scatter (K3Puf + gamma plot) or both. The scatter in the K3Puf + gamma plot is a result of the small sample size inherent in cytochrome b sequences (1,041 bases); were the sequences longer, it would have been reduced. Conversely, the relative lack of scatter in the DNA hybridization plot is due to the fact that DNA hybridization distances are based on the comparison of tens of thousands, if not millions, of base pairs.
Rates of Evolution
Perhaps the most interesting discovery of our analysis is that heron nuclear and mitochondrial DNAs display similar underlying lineage-based rates of evolution. This discovery adds to a growing body of evidence to this effect. Martin (1999)
discovered the same phenomenon when he compared shark trees inferred from nuclear RAG-1 and mitochondrial cytochrome b genes. Mindell et al. (1996)
found that nuclear and mitochondrial protein-coding genes have evolved, in general, more slowly in chickens (Gallus gallus) than in representative mammals (Homo sapiens, Mus musculus, and Rattus novegicus). Preliminary molecular comparisons of tubenosed birds (Procellariiformes) suggest that both scnDNA and the cytochrome b gene evolve more slowly in clades consisting of large-bodied, as opposed to small-bodied, species (Sibley and Ahlquist 1990
; Nunn and Stanley 1998
). Similar results have been found in comparisons of mammalian orders consisting mainly of large- versus small-bodied species (Martin and Palumbi 1993
).
A variety of causes have been suggested to account for molecular rate variation, including differences in metabolic rate, generation time, rate of germ cell division, body temperature, DNA repair efficiency, population sizes, and clade size (reviewed by Martin and Palumbi 1993
; Rand 1994
; Omland 1997
; Bleiweiss 1998
). For herons, we lack data on most of these suspected causes. However, because several of the potential causes, such as metabolic rate and generation time, are correlated with body size (Martin and Palumbi 1993
; Bleiweiss 1998
), we can look for a relationship between body size and molecular rate as an approximate indicator of cause. A quick examination of the herons, however, reveals that body size does not explain their molecular rate pattern. For example, the fast-evolving bitterns include of some of the largest (Botaurus spp.) as well as some of the smallest (Ixobrychus spp.) heron species. Another potential cause of rate variation, clade size, is also easily examined for the herons. Speciose clades are expected to exhibit faster rates of molecular evolution than depauperate clades because of the genetic sampling phenomena (drift, bottlenecks, etc.) and potential "genetic revolutions" (Mayr 1963
) associated with speciation (Omland 1997
). A relationship between evolutionary and speciation rates has been proposed many times based on taxonomic patterns (e.g., Eldredge and Gould 1972
) and genetic studies (e.g., Nichol, Rowe, and Fitch 1993
; Barraclough, Harvey, and Nee 1996
; Moran 1996
). In herons, the most speciose cladesbitterns (12 species of Botaurus and Ixobrychus) and true egrets (11 species of Egretta)appear to have evolved the fastest. Conversely, depauperate cladestiger herons (five species) and boat-billed heron (1 species)appear to have evolved slowly. Unfortunately, this ratetoclade size relationship is difficult to quantify in herons because, even if we had sampled all of the species, there would not have been enough clades exhibiting alternative species numbers and rates to test repetitive patterns by comparative methods. Moreover, we have no idea of the historical diversity of heron clades (i.e., how much extinction they have experienced).
A simple causal explanation for rate variation in birds remains elusive, in part because of a dearth of data, but also because different groups may have been influenced by different forces. In an unusually careful demonstration, Bleiweiss (1998)
found that lineage-based rates of scnDNA evolution in hummingbirds are correlated with metabolic rates, but Mindell et al. (1996)
argued that metabolism could not be responsible for rate differences between birds and mammals based on comparisons of nuclear and mitochondrial protein-coding and ribosomal genes. These two studies compared taxa on very different hierarchical levels, and patterns observed between classes of vertebrates may not be expected to occur within classes. Moreover, even within the class Aves, rates of molecular evolution in different orders could be influenced by different factors. One would predict, for example, that metabolism should be an important force in the evolution of hummingbirds (Rand 1994
), but metabolism seems less likely to be important in herons and tubenoses. As we gather more data on rates of evolution in closely related birds, the accuracy of these predictions should be revealed.
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Acknowledgements |
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Footnotes |
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1 Keywords: Ardeidae
congruence analysis
cytochrome b sequence
DNA-DNA hybridization
phylogeny
rates of evolution
2 Address for correspondence and reprints: Frederick H. Sheldon, Museum of Natural Science, 119 Foster Hall, Louisiana State University, Baton Rouge, Louisiana 70803. E-mail: fsheld{at}lsu.edu
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