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Response to Comment on "Hexapod Origins: Monophyletic or Paraphyletic?"

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Francesco Nardi at Università degli Studi di Siena
Francesco Nardi
Giacomo Spinsanti at Università degli Studi di Siena
Giacomo Spinsanti
Jeffrey Boore at Phenome Health
Jeffrey Boore
  • Phenome Health
Antonio Carapelli at Università degli Studi di Siena
Antonio Carapelli
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Abstract and Figures

Assessing the relationships among arthropod taxa is an intensely debated issue in metazoan phylogeny, with various studies testing different character sets, phylogenetic methods, and strategies for analyzing molecular data ( [1][1]–[3][2] ). Delsuc et al. ( [4][3] ) criticize our recent hypothesis
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Response to Comment on
“Hexapod Origins: Monophyletic
or Paraphyletic?”
Assessing the relationships among arthropod
taxa is an intensely debated issue in metazoan
phylogeny, with various studies testing dif-
ferent character sets, phylogenetic methods,
and strategies for analyzing molecular data
(1–3). Delsuc et al. (4) criticize our recent
hypothesis that Hexapoda is not monophylet-
ic (3) on methodological grounds, including
use of a suboptimal substitution matrix, lack
of correction for among-site rate variation
(ASRV), and biased taxon selection. They fur-
ther introduce a method (5) that recodes nucle-
otide sequences into only two categories—
purines (R) an d pyrimidines (Y)—and use a
maximum-likelihood approach to reanalyze
our data recoded in this fashion. They claim
that this method corrects for artefac-
tual clustering of taxa that results from
compositional bias of nucleotide con-
tent; this view is bolstered by the cor-
rect placement of the honeybee and
louse, which were anomalously placed
in our tree and others (1, 6, 7), within
Insecta. Their reanalysis places col-
lembolans at the base of Hexapoda,
although with moderate to low sup-
port, and thus questions the main con-
clusion of our study.
Despite the correct placement of
the honeybee and louse, it is not clear
that the Delsuc et al. method performs
better generally. In fact, one might
expect that reducing nucleotide se-
quence data set to only two states (R
and Y) might exacerbate saturation at
many sites, and be more susceptible to
problems of nonstationarity of substitu-
tions than an amino acid data set (8). In
the latter, the model of substitution re-
flects the probability of a replacement to
be fixed, and the use of 20-state charac-
ters decreases the possibility of over-
looking convergence. The inference of
phylogenies based on amino acid se-
quences is common practice and is gen-
erally accepted as among the most reli-
able of methods (8 –10). Although the
matrix of amino acid change used in the
first of our two analyses was based on
vertebrate sequences, it has been exten-
sively used to study relationships among
invertebrates with no reports of signifi-
cant flaws (1, 6).
In our previous study (3), we used an
alignment of amino acid sequences and two
likelihood-based methods of analysis: A clas-
sical likelihood reconstruction using a fixed-
parameter model of amino acid substitution,
and a Bayesian analysis based on a general
time reversible (GTR) model of substitution
and modeling rate variation across sites using
an invariant ⫹⌫distribution. Both analyses
converged on the same topology, which sup-
ports the placement of Collembola outside of
the Insecta ⫹Crustacea assemblage.
The correction for rate variation among
sites has been shown to potentially affect
estimates of branch lengths and divergence
times, but it seems to have only a limited
effect on topology (11). To further address
this issue, we calculated the likelihood of
competing trees under the same matrix, but
modeled ASRV using a ⌫distribution (12).
Table 1 shows that the trees we produce (with
Collembola outside Insecta ⫹Crustacea)
give higher likelihood scores, although with
different degrees of significance, regardless
of the use of ⌫correction.
To investigate the possible effects of tax-
on exclusion on the analysis, we repeated the
analysis described in (3) on the 25-taxon data
set of Delsuc et al. (4). To rule out the
possibility that the analysis is negatively af-
fected by use of a suboptimal substitution
matrix and lack of ASRV correction, we used
the Bayesian method outlined in (3) (Fig. 1).
Again, Collembola fall outside the Insecta ⫹
Crustacea clade, although with only mo-
derate support.
Our past (3) and present analyses, the
analysis of Delsuc et al. (4), as well as
other molecular studies (13) demonstrate
that a reliable reconstruction of the phylog-
eny of Arthropoda—and the assessment of
the mono- or paraphyly of Hexapoda,
specifically—are still disputable. Re-
sults differ when subjecting the same
data set to different methods of anal-
ysis or when using different subsets of
data with the same methods. This
leaves the impression that none of the
competing hypotheses can yet be re-
jected with certainty. However, we
believe that the theory of hexapod
nonmonophyly proposed by several
studies (3, 7, 14, 15) must be consid-
ered. In this context, the recent discov-
ery of a marine hexapod from the
Lower Devonian (16) undermines the
traditional association between terres-
trialization and the evolution of hexa-
pods, leaving room for alternative hy-
potheses concerning hexapod origins.
Francesco Nardi
Giacomo Spinsanti
Department of Evolutionary Biology
University of Siena
via Aldo Moro 2
53100 Siena, Italy
E-mail: nardifra@unisi.it
Jeffrey L. Boore
U.S. Department of Energy Joint
Genome Institute and Lawrence
Berkeley Laboratory
Walnut Creek, CA 94598, USA
Antonio Carapelli
Romano Dallai
Francesco Frati
Department of Evolutionary Biology
University of Siena
Fig. 1. Maximum likelihood tree obtained applying the
method outlined in (3) as implemented in MrBayes ver. 2.1
(20) (aamodel ⫽gtr; rates ⫽invgamma) to the 25-taxon
data set of Delsuc et al. (4). The analysis was run for
570,000 generations and sampled every 100 generations.
The first 150,000 generations were excluded from the
analysis as the burn-in of the search. Numbers at each node
indicate posterior probabilities. Branch lengths are drawn
according to estimates obtained with PAML.
TECHNICAL COMMENT
www.sciencemag.org SCIENCE VOL 301 12 SEPTEMBER 2003 1482e
References and Notes
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19. This methodology, as implemented in PAML (12), is
unfortunately not suitable to conduct a full likelihood
search. However, it is efficient for comparing a lim-
ited number of trees.
20. The amino acid substitution model “gtr,” present as an
option in MrBayes 2.1, has not been implemented, in its
original form, in the latest release MrBayes 3. It is not
clear to us if the method is still available under a
different set of commands or if it has been removed
altogether.
21. We thank P. Lio` for useful discussion on this topic.
4 June 2003; accepted 18 August 2003
Table 1. Comparison of tree topologies under the amino acid substitution model mtREV24 implemented
in PAML (12, 19) and incorporating a ⌫-correction for ASRV [pKH ⫽Pvalue of the Kishino-Hasegawa test
(17); pSH ⫽Pvalue of the Shimodaira-Hasegawa test (18); pRELL ⫽Pvalue of the RELL bootstrap (17 )].
In the 15-taxon data set, the topology derived in Nardi et al. (3) is compared with a topology derived in
Delsuc et al. (4), after pruning extra taxa and exchanging Anopheles gambiae with A. quadrimaculatus.In
the 25-taxon data set, the topology from Fig. 1 is compared with the topology derived in (4). In the
35-taxon data set, the two topologies derived in (3) and (4) are compared.
Tree Likelihood alpha (of ⌫) pKH (17) pSH (18) pRELL (17)
15 taxa Nardi et al. ⫺18488.559 0.42838 1.000 1.000 0.914
Delsuc et al. ⫺18507.904 0.42228 0.087 0.090 0.086
25 taxa Nardi et al. ⫺25482.424 0.41111 1.000 1.000 0.883
Delsuc et al ⫺25492.299 0.41063 0.121 0.119 0.117
35 taxa Nardi et al. ⫺34838.359 0.47124 1.000 1.000 0.920
Delsuc et al ⫺34881.787 0.45337 0.077 0.076 0.080
TECHNICAL COMMENT
12 SEPTEMBER 2003 VOL 0 SCIENCE www.sciencemag.org1482e
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... Haas et al. (2003) did not consider other hypotheses such as the Pancrustacea or Tetraconata concept that suggest a monophyletic Crustacea and Hexapoda clade excluding the Myriapoda, based on morphological, developmental , and molecular evidence (e.g. ZrzavyándZrzavyánd Stys 1997; Dohle 2001; Schram and Jenner 2001; Richter 2002; Nardi et al. 2003; Mallatt et al. 2004; Klass 2007). But not only are the phylogenetic relationships of Hexapoda still a matter of discussion, their monophyly (discussed by, e.g., Hennig 1969; Kristensen 1998; Willmann 1998; Ax 1999; Klass and Kristensen 2001; Willmann 2003; Bitsch and Bitsch 2004; Mallatt et al. 2004) also has been doubted repeatedly (e.g. ...
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The Devonian Hunsrück Slate fossil Devonohexapodus bocksbergensis Haas, Waloszek & Hartenberger, 2003 has been interpreted as a stem-lineage representative of the Hexapoda, implying their marine origin and independent terrestrialisation within the ‘Atelocerata’. Devonohexapodus bocksbergensis was based on a single specimen embedded in a lateral position. Reinvestigation of that holotype and of all known specimens of the Hunsrück Slate arthropod Wingertshellicus backesi Briggs & Bartels, 2001 demonstrates that all this material represents a single species. The latter is redescribed, its taxonomic diagnosis is emended, and the name Devonohexapodus bocksbergensis is treated as a junior synonym of Wingertshellicus backesi. The phylogenetic position of W. backesi neither is that of a stem-lineage representative of Hexapoda, nor does it fall within the crown group Mandibulata. The Hunsrück Slate provides no evidence of an independent terrestrialisation within the ‘Atelocerata’ or of a marine origin of the Hexapoda.
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... This result seemed to support the view that there can be more phylogenetic information within the nucleotide data than could be recovered with amino acids. Nardi et al. (2003b) responded to this critique by reafÞrming the value of amino acids and by demonstrating the persistent recovery of a diphyletic Hexapoda even after accounting for rate heterogeneity among sites and biases in taxon sampling. They summarized by stating that hexapod diphyly is one of several competing hypotheses that must be tested by further evidence, but that even now it is consistent with one fossil and the results of some molecule-based studies; that is, their own work (Nardi et al. 2001, 2003a) and a tendentious interpretation of the ambiguous results of one study based on 18S rDNA (Spears and Abele 1997) In defending their hypothesis, Nardi et al. 2003b noted fossils of a presumed marine stem hexapod, ...
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... Given their ecological ubiquity and phylogenetic position, understanding the genetic basis of Collembola's key traits is crucial to understanding their success and that of more derived hexapod groups such as ectognathous insects. The placement of Collembola within the arthropods is a particular problem that morphological analyses [4,5] and complete mitochondrial genome sequences (see [6]) have failed to conclusively resolve, with efforts now shifting to analysis of whole genomes and transcriptomes (e.g., [2,[7][8][9][10]). Resolving the placement of Collembola would allow a better understanding of the origins and evolution of Insecta, the colonisation of land by arthropods and the evolution of key traits within Collembola and more generally across Hexapoda. ...
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... Recent mtgenome phylogenetic studies of insects have recovered unexpected relationships, but with high branch support. For example, an unexpected relationship between Crustacea and Collembola leading to a paraphyletic Hexapoda based on mtgenome data (Nardi et al., 2003a) spurred controversy (Delsuc et al., 2003;Nardi et al., 2003b), and a more thorough analysis suggested that mtgenome data alone contain inadequate signal to resolve this relationship unambiguously (Cameron et al., 2004). Within Insecta, Stewart & Beckenbach (2003) found Orthoptera (Locusta) to group with Hemiptera, Lepidoptera, or to be a sister group to the rest of the holometabolous orders, depending on the analytical treatment used. ...
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... The result accords with previous morphological evidence. However, in a response to Delsuc et al. and using an additional analysis, Nardi et al. (2003b) maintain their view on the possible nonmonophyly of hexapods. ...
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Full-text available
  • Jul 2000
The complete sequence of the mitochondrial genome of the giant tiger prawn, Penaeus monodon (Arthropoda, Crustacea, Malacostraca), is presented. The gene content and gene order are identical to those observed in Drosophila yakuba. The overall AT composition is lower than that observed in the known insect mitochondrial genomes, but higher than that observed in the other two crustaceans for which complete mitochondrial sequence is available. Analysis of the effect of nucleotide bias on codon composition across the Arthropoda reveals a trend with the crustaceans represented showing the lowest proportion of AT-rich codons in mitochondrial protein genes. Phylogenetic analysis among arthropods using concatenated protein-coding sequences provides further support for the possibility that Crustacea are paraphyletic. Furthermore, in contrast to data from the nuclear gene EF1alpha, the first complete sequence of a malacostracan mitochondrial genome supports the possibility that Malacostraca are more closely related to Insecta than to Branchiopoda.
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The Complete Mitochondrial DNA Sequence of the Basal Hexapod Tetrodontophora bielanensis: Evidence for Heteroplasmy and tRNA Translocations
Article
Full-text available
  • Aug 2001
We present the complete 15,455-nt mitochondrial DNA sequence of the springtail Tetrodontophora bielanensis (Arthropoda, Hexapoda, Collembola). The gene content is typical of most metazoans, with 13 protein-coding genes (PCGs), 2 genes encoding for ribosomal RNA subunits, and 22 tRNA genes. The nucleotide sequence shows the well-known A+T bias typical of insect mtDNA; its A+T content is lower (72.7%) than that observed in other insect species, but still higher than that in other arthropodan taxa. The bias appears to be uniform across the whole molecule, unlike other insect taxa, which show increased A+T content in the so-called A+T-rich region. However, the bias is slightly higher in the third codon positions of the PCGs (81.4%). Anomalous initiation codons have been observed in the nad2 and the cox1 genes. In the latter, the ATTTAA hexanucleotide is suggested to be involved in the initiation signaling. All tRNAs could be folded into the typical cloverleaf secondary structure, but the tRNA for cysteine appears to be missing the DHU arm. Long tandemly repeated regions (193 nt) were found in the A+T-rich region, which in turn was shown to have the possibility of forming a complex array of secondary structures. One of these structures encompassed the junction between the repeats. The A+T-rich region was also interesting in that it showed heteroplasmy in the number of repeats. Three haplotypes were found, possessing 2, 3, and 4 identical repeats, respectively. The order of protein coding and rRNA genes in the molecule was determined and was identical to that of all insects studied so far. However, two tRNA translocations were found which were unprecedented among Arthropoda. These involved the trnQ, which was found between the rrnS and the A+T-rich region, and the trnS(ucn), which was located between trnM and trnI. A preliminary phylogenetic analysis based on the amino acid sequence of the PCGs failed to find support for the monophyly of Hexapoda.
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Arthropod phylogeny based on eight molecular loci and morphology
Article
Full-text available
  • Oct 2001
The interrelationships of major clades within the Arthropoda remain one of the most contentious issues in systematics, which has traditionally been the domain of morphologists. A growing body of DNA sequences and other types of molecular data has revitalized study of arthropod phylogeny and has inspired new considerations of character evolution. Novel hypotheses such as a crustacean-hexapod affinity were based on analyses of single or few genes and limited taxon sampling, but have received recent support from mitochondrial gene order, and eye and brain ultrastructure and neurogenesis. Here we assess relationships within Arthropoda based on a synthesis of all well sampled molecular loci together with a comprehensive data set of morphological, developmental, ultrastructural and gene-order characters. The molecular data include sequences of three nuclear ribosomal genes, three nuclear protein-coding genes, and two mitochondrial genes (one protein coding, one ribosomal). We devised new optimization procedures and constructed a parallel computer cluster with 256 central processing units to analyse molecular data on a scale not previously possible. The optimal 'total evidence' cladogram supports the crustacean-hexapod clade, recognizes pycnogonids as sister to other euarthropods, and indicates monophyly of Myriapoda and Mandibulata.
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Exploring Among-Site Rate Variation Models in a Maximum Likelihood Framework Using Empirical Data: Effects of Model Assumptions on Estimates of Topology, Branch Lengths, and Bootstrap Support
Article
Full-text available
  • Mar 2001
We have investigated the effects of different among-site rate variation models on the estimation of substitution model parameters, branch lengths, topology, and bootstrap proportions under minimum evolution (ME) and maximum likelihood (ML). Specifically, we examined equal rates, invariable sites, gamma-distributed rates, and site-specific rates (SSR) models, using mitochondrial DNA sequence data from three protein-coding genes and one tRNA gene from species of the New Zealand cicada genus Maoricicada. Estimates of topology were relatively insensitive to the substitution model used; however, estimates of bootstrap support, branch lengths, and R-matrices (underlying relative substitution rate matrix) were strongly influenced by the assumptions of the substitution model. We identified one situation where ME and ML tree building became inaccurate when implemented with an inappropriate among-site rate variation model. Despite the fact the SSR models often have a better fit to the data than do invariable sites and gamma rates models, SSR models have some serious weaknesses. First, SSR rate parameters are not comparable across data sets, unlike the proportion of invariable sites or the alpha shape parameter of the gamma distribution. Second, the extreme among-site rate variation within codon positions is problematic for SSR models, which explicitly assume rate homogeneity within each rate class. Third, the SSR models appear to give severe underestimates of R-matrices and branch lengths relative to invariable sites and gamma rates models in this example. We recommend performing phylogenetic analyses under a range of substitution models to test the effects of model assumptions not only on estimates of topology but also on estimates of branch length and nodal support.
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Hexapod Origins: Monophyletic or Paraphyletic?
Article
Full-text available
  • Apr 2003
  • SCIENCE
Recent morphological and molecular evidence has changed interpretations of arthropod phylogeny and evolution. Here we compare complete mitochondrial genomes to show that Collembola, a wingless group traditionally considered as basal to all insects, appears instead to constitute a separate evolutionary lineage that branched much earlier than the separation of many crustaceans and insects and independently adapted to life on land. Therefore, the taxon Hexapoda, as commonly defined to include all six-legged arthropods, is not monophyletic.
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Devonohexapodus bocksbergensis, a new marine hexapod from the Lower Devonian Hunsr??ck Slates, and the origin of Atelocerata and Hexapoda
Article
  • Dec 2003
We describe a new arthropod (approximately 75 mm long) from the Lower Devonian (Lower Emsian) Hunsrück Slates near Bundenbach, western Germany. The specimen is from an isolated piece of rock found on the quarry dump, precluding precise resolution of stratigraphic age. The Hunsrück Slates are marine sediments with a rich fauna of exclusively marine taxa, suggesting that our fossil was also marine. The animal has a small head with large compound eyes and long, filiform, myocerate antennae. Its trunk is divided distinctly into a thorax with three segments and three pairs of slender legs, and a post-thoracic domain composed of 35-40 limb-bearing segments of which the anteriormost are paired, stout, and ventrally-oriented leglets; the three ultimate limb-bearing segments bear longer, posteriorly-oriented and apparently specialised appendages. The overall appearance of the new form is reminiscent of Archaeognatha or Odonata. It is interpreted as a representative of the Hexapoda because of the possession of a three-segmented thorax and three pairs of legs that are clearly distinct from the posterior set. The large number of leg-bearing post-thoracic segments discriminates it from the Insecta, which possess 11 “abdominal” segments maximally, originally also leg-bearing. The formal systematic classification of the organism is: (Hexapoda (Devonohexapodus bocksbergensis + Insecta (“entognaths” + Ectognatha))). The morphology of the fossil and its environment suggest that the hexapody of hexapods did not evolve as an adaptation to terrestrial locomotion, but was already developed in the marine habitat. No terrestrial arthropods have changed their original tagmosis for biomechanical reasons, for example, no “myriapods” have reduced their leg numbers or modified their trunk to evolve a thorax and abdomen similar to insects. Walking exclusively on uniramous prosomal legs in the Chelicerata also occurred well before terrestrialization of this other euarthropodan group. It is not unlikely that the last common ancestor of the Hexapoda was large and that the small size of extant “entognaths” evolved due to reduction in their stem lineage. Being marine, the new fossil also has considerable impact on hypotheses about the early evolution of Atelocerata (“myriapods” + Hexapoda). For example, if their last common ancestor was aquatic, terrestrialization took place at least twice and tracheal breathing probably evolved independently in both taxa after terrestrialization.
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Molecular phylogenetics: state-of-the-art methods for looking into the past
Article
  • Jun 2001
  • TRENDS GENET
As the amount of molecular sequence data in the public domain grows, so does the range of biological topics that it influences through evolutionary considerations. In recent years, a number of developments have enabled molecular phylogenetic methodology to keep pace. Likelihood-based inferential techniques, although controversial in the past, lie at the heart of these new methods and are producing the promised advances in the understanding of sequence evolution. They allow both a wide variety of phylogenetic inferences from sequence data and robust statistical assessment of all results. It cannot remain acceptable to use outdated data analysis techniques when superior alternatives exist. Here, we discuss the most important and exciting methods currently available to the molecular phylogeneticist.
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Mitochondrial protein phylogeny joins myriapods with chelicerates
Article
  • Oct 2001
The animal phylum Arthropoda is very useful for the study of body plan evolution given its abundance of morphologically diverse species and our profound understanding of Drosophila development. However, there is a lack of consistently resolved phylogenetic relationships between the four extant arthropod subphyla, Hexapoda, Myriapoda, Chelicerata and Crustacea. Recent molecular studies have strongly supported a sister group relationship between Hexapoda and Crustacea, but have not resolved the phylogenetic position of Chelicerata and Myriapoda. Here we sequence the mitochondrial genome of the centipede species Lithobius forficatus and investigate its phylogenetic information content. Molecular phylogenetic analysis of conserved regions from the arthropod mitochondrial proteome yields highly resolved and congruent trees. We also find that a sister group relationship between Myriapoda and Chelicerata is strongly supported. We propose a model to explain the apparently parallel evolution of similar head morphologies in insects and myriapods.
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Modeling Mitochondrial Protein Evolution Using Structural Information
Article
  • May 2002
We present two new models of protein sequence evolution based on structural properties of mitochondrial proteins. We compare these models with others currently used in phylogenetic analyses, investigating their performance over both short and long evolutionary distances. We find that our models that incorporate secondary structure information from mitochondrial proteins are statistically comparable with existing models when studying 13 mitochondrial protein data sets from eutherian mammals. However, our models give a significantly improved description of the evolutionary process when used with 12 mitochondrial proteins from a broader range of organisms including fungi, plants, protists, and bacteria. Our models may thus be of use in estimating mitochondrial protein phylogenies and for the study of processes of mitochondrial protein evolution, in particular for distantly related organisms.
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