Molecular Biology and Evolution 18:1604-1609 (2001)
© 2001 Society for Molecular Biology and Evolution
A Major Mitochondrial Gene Rearrangement Among Closely Related Species
Department of Biological Sciences, Florida International University
Department of Zoology, Field Museum of Natural History, Chicago, Illinois
The sequential order of genes in animal mitochondrial DNA tends to be conserved at high taxonomic levels. Consequently, when mitochondrial gene rearrangements occur, they can provide compelling markers of ancient phylogenetic history (see reviews in Boore, Daehler, and Brown [1999]
, Saccone et al. [1999]
, and references therein). Such gene order characters have proven particularly useful for resolving deep-branching events characterizing superphyla, phyla, and classes, a scale over which nucleotide sequence analysis has often proven problematic (e.g., Smith et al. 1993
; Boore and Brown 1994a, 1998, 2000
; Boore et al. 1995
; Boore, Lavrov, and Brown 1998
; Stechmann and Schlegel 1999
). Most frequently, these rearrangements are associated with the movement of tRNA genes which, based on their stem-and-loop structure, may also have an underlying role as mobilizing elements within the mitochondrial genome (Moritz and Brown 1987
; Stanton et al. 1994
; Saccone et al. 1999
). Gene rearrangements involving ribosomal and protein-encoding genes (hereinafter referred to as "major" genes), however, are much rarer. Here we report a mitochondrial gene rearrangement involving major genes that has occurred within a genus of marine vermetid gastropods that diversified within the Cenozoic. Based on data from the fossil record and an independent molecular calibration, we estimate that this gene order change may have occurred within the last 38–48 Myr, making this a very recent major gene order rearrangement. This finding thus has important implications for the use of gene order characters in metazoan phylogeny, in terms of both understanding the mechanism of gene order rearrangements and determining the taxonomic level and timescale over which these major rearrangements may prove useful.
The family Vermetidae comprises seven genera with 
100 extant species of sessile, uncoiled, suspension-feeding gastropods found in shallow marine waters in warm temperate to tropical latitudes throughout the world (Keen 1961
; Morton 1965
; unpublished data). Based on our current understanding of gastropod evolution, vermetid gastropods radiated from a basal caenogastropod stock sometime in the early Cenozoic (Keen 1961
; unpublished data). As part of a study to investigate evolutionary relationships within this group, we amplified and sequenced an 1,800-bp stretch of mitochondrial DNA for six vermetid species within the genus Dendropoma, as well as two representatives of the related vermetid genus Serpulorbis. This amplification product spanned domains III–IV of the small-subunit rRNA (rrnS), an intervening tRNA valine (trnV), and domains I–IV of the large-subunit rRNA (rrnL). In four of six Dendropoma species sampled, the PCR product was 700 bp larger than expected (fig. 1A and B
). We sequenced these amplification products and subsequently determined that two tRNA genes (trnK and trnP) and the gene encoding subunit 6 of the NADH dehydrogenase complex (nad6) had been inserted between the trnV and rrnL genes in Dendropoma petraeum, Dendropoma corrodens, Dendropoma gregarium, and Dendropoma nebulosum (fig. 1B
). Further investigation of two of these species (D. gregarium and D. nebulosum) demonstrated that both the trnP and the nad6 genes were not present in the ancestral position, downstream of the rrnL gene (fig. 1B
). The ancestral condition was determined by comparison with Dendropoma maximum and Serpulorbis aureus within the vermetids and, more broadly, by comparison with other mollusks, including a caenogastropod, Littorina (Wilding, Mill, and Grahame 1999
); a chiton, Katharina (Boore and Brown 1994b
); and a cephalopod, Loligo (Tomita 1998
). Subsequent analyses of vermetid relationships based on nucleotide sequence data from rrnS, trnV, and rrnL indicated that this novel gene order was a derived event that occurred within the evolution of a monophyletic clade of Dendropoma (fig. 1A
).
|
and 
, respectively. Subsequent amplification and sequencing of a fragment spanning from the rrnL to the cob gene were performed for Dendropoma maximum, D. gregarium, and D. nebulosum to identify the order of downstream genes within specific clades using newly designed primers: 16SF (5'-TTGYGACCTCGATGTTGGA-3') and SUP3 (5'-ACCTAGTAAAGAACCAAAATTTCATCA-3'). Approximate locations of the forward 16SF and SUP3 primers are indicated by the symbols 
and 
, respectively. Amplification of this region and partial sequencing of downstream genes has also been completed for S. aureus. The rRNA genes were identified by their similarity in sequence and secondary structure to other molluscan mitochondrial rrnS and rrnL genes. Protein-encoding genes were identified by the presence of an uninterrupted open reading frame ending in a full or truncated stop codon and by nucleotide and amino acid similarity to published mitochondrial gene sequences. Identification of tRNAs was based on the ability to fold these sequences into cloverleaf-like structures characteristic of tRNA molecules; specific identities were based on the triplet sequence in their putative anticodon loops. The gene order present in D maximum and S. aureus has also been recorded in other caenogastropod taxa (e.g., Littorina [Wilding, Mill, and Grahame 1999]While the dynamics of gene rearrangements have rarely been examined in detail within invertebrate lineages (but see Yamazaki et al. 1997
; Arndt and Smith 1998
; Campbell and Barker 1999
; Dowton and Austin 1999
), most vertebrate mitochondrial gene rearrangements can be explained by tandem duplication following slipped-strand mispairing during replication or the accidental recognition of alternate sites for initiation or termination of light-strand replication. If the gene rearrangement within Dendropoma resulted from tandem duplication of the region spanning from rrnL to cob, with subsequent deletion of duplicate genes, one would expect to find sequence remnants, otherwise uncommon in animal mitochondrial DNA, marking the former positions of at least some of the duplicated genes. Indeed, noncoding sequences are apparent between trnV and trnK (12–16 bp, n = 4), trnK and trnP (19–55 bp, n = 4), and protein-encoding genes nad1 and cob (9–70 bp, n = 3) in the animals that have undergone the rearrangement. A duplication event involving only these genes, however, cannot explain the translocation of trnK to a position between trnV and trnP. Consequently, either additional genes upstream of the rRNA genes were also involved in this duplication event, or some other mechanism of tRNA translocation must be invoked.
We investigated the timing of this gene rearrangement employing our robust, well-resolved phylogeny and the fossil record of the Vermetidae. The earliest dated fossil occurrence of Dendropoma is 24 MYA (Aquitanian, Miocene; Keen 1961
), although a recent undated Oligocene occurrence (Bandel and Kowalke 1997
) with a larval shell morphology similar to extant Dendropoma species may extend this to 38 MYA. A proposed even-older, "early Dendropoma" from the Eocene of Gan (southern France; Bandel and Kowalke 1997
), however, differs greatly in larval shell sculpture, and consequently the placement of the taxon in Dendropoma is questionable. Currently, therefore, the fossil record indicates that this rearrangement must have occurred during the radiation of Dendropoma within the past 38 Myr.
To provide an estimate independent of the fossil record, we also dated this rearrangement based on levels of sequence divergence between Dendropoma with plesiomorphic versus apomorphic gene arrangements. For this, we calibrated rates of sequence divergence within the conservatively aligned portions of our mitochondrial DNA data set using sequence divergence measured between three geminate species pairs of caenogastropods (Plicopurpura pansa/columellaris and Plicopurpura patula; Melongena melongena and Melongena patula; Vasum caestus and Vasum muricatum; Vermeij 1978
) isolated by the Pliocene emergence of the Isthmus of Panama around 3.5 MYA (Vermeij 1978
; Keigwin 1982
). To accomplish this, sequence data from each species pair were aligned using Clustal X (Jeanmougin et al. 1998
), and then each data set was consecutively aligned to a profile alignment of Dendropoma/Serpulorbis (described in fig. 1A
). The final alignment was adjusted by hand according to secondary-structure models of these genes, and regions of ambiguous alignment were excluded, resulting in a conservative data set of 1,182 characters within a total alignment of 1,953 characters. Pairwise distances between all taxa were adjusted for multiple hits using the HKY85+
model of evolution with PINV = 0.36 and 
= 1.48 (Posada and Crandall 1998), estimated previously for the Dendropoma/Serpulorbis data set. Adjusted pairwise sequence divergences among geminate pairs were then used to determine the relation between sequence divergence and time since divergence using a weighted linear regression and constraining the line through the origin (Hillis, Mable, and Moritz 1996
). Using this relationship, we extrapolated the estimated time of divergence from adjusted measures of pairwise differences between Dendropoma species. This estimate dated the most recent common ancestor of the Dendropoma species sampled to 47.9 MYA ± 38.5 Myr (±95% confidence interval), close to estimates derived from the fossil record. Acceptance of an earlier divergence date for some geminate pairs, as has been suggested by some authors (Knowlton and Weigt 1998
), would result in an older date of divergence between the Dendropoma clades with and without the mitochondrial gene order rearrangement and less congruence with the fossil record of Dendropoma.
Although the major gene order rearrangement within Dendropoma appears to be recent relative to other documented cases, few other studies have been able to provide as well constrained an estimate of the timing of this event as we report here. Potentially recent major gene order rearrangements have been documented within the crustacean order Decapoda (Hickerson and Cunningham 2000)
, the gastropod superfamily Helicoidea (Yamazaki et al. 1997
), the parasitic flatworm genus Schistosoma (Le et al. 2000)
, and the tick family Ixodidae (Black and Roehrdanz 1998
; Campbell and Barker 1998
). Alternative interpretations of a major gene rearrangement recently described within the bird order Passeriformes (Mindell, Sorenson, and Dimcheff 1998
; Bensch and Härlid 2000
) do not require rearrangement of major genes (Boore and Brown 1998
), so this case will not be considered further. Since the phylogenetic distribution of gene rearrangements has yet to be investigated extensively within either decapod crustaceans or helicoidean gastropods, the timing of these changes in gene order is unclear. In contrast, the major gene order rearrangement within the genus Schistosoma appears to be confined to a largely African lineage of parasitic worms associated with the snail hosts Biomphalaria and Bulinus (Le et al. 2000)
. Differences in nucleotide sequence, karyotype, morphology, and life history characteristics between members of this lineage and the other major lineage of Schistosoma from East Asia (Déspres et al. 1992
; Barker and Blair 1996
) suggest a deep phylogenetic divide between these two groups; however, the lack of a fossil record for schistosomes has prevented the dating of this divergence. Attempts to date this split by calibrating rates of molecular evolution within schistosome clades (see Déspres et al. 1992
) have used an unreliable vertebrate (mouse/rat) calibration point (see Kumar and Hedges [1998]
and Yoder and Yang [2000]
for markedly different calibrations) and thus remain speculative at best. If, as suggested by Davis (1980)
, the divergence of the Asian lineage of Schistosoma occurred during the separation of the Indian subcontinent from Africa, then this gene rearrangement may have occurred within the past 70–148 Myr (see Déspres et al. 1992
), although other scenarios are also possible. Finally, extensive sampling within the tick family Ixodidae and the construction of a robust phylogeny for this group have helped to narrow the distribution of this gene rearrangement to four subfamilies of metastriate ticks (Black and Roehrdanz 1998
; Dobson and Barker 1999
). Attempts to date this rearrangement directly have been stymied by the lack of a good fossil record for this family, and estimates based on different biogeographic scenarios vary widely. Some biogeographic interpretations place this rearrangement prior to the breakup of Pangea more than 210 MYA (Campbell and Barker 1999
; Dobson and Barker 1999
), while others suggest that this may have occurred sometime in the early Cretaceous, approximately 130–140 MYA (Klompen et al. 2000)
. Given these poorly constrained estimates of the timing of these gene order rearrangements, directed efforts should now focus on the broad taxonomic sampling of major mitochondrial gene orders within lineages with good fossil records and robust phylogenies in order to understand the timing and tempo of major gene order changes throughout metazoan evolution.
The gene rearrangement within Dendropoma is intriguing not only because of the potential recency of this event, but also because of the genes involved. Gene order changes involving protein-encoding and ribosomal RNA genes are rare events within most animal phyla. Over more than 500 Myr of arthropod evolution, for instance, all known gene rearrangements except those within one lineage of ticks (Black and Roehrdanz 1998
; Campbell and Barker 1998
) and decapods (Hickerson and Cunningham 2000)
have involved translocations of tRNA genes alone (Boore 1999
). Likewise, the mitochondrial gene order of the cephalochordate Branchiostoma floridae differs from the typical mammalian arrangement solely in the position of four tRNAs (Boore, Daehler, and Brown 1999
). In contrast, the phylum Mollusca has long been known to exhibit an exceptionally variable arrangement of genes within mitochondrial DNA (e.g., Boore and Brown 1994a
; Yamazaki et al. 1997
; Boore 1999
; Kurabayashi and Ueshima 2000
). Mitochondrial genomes from representatives of three classes of molluscs have remarkably few shared gene boundaries in common (Yamazaki et al. 1997
), and gene order also varies extensively even within the class Gastropoda (Yamazaki et al. 1997
; Kurabayashi and Ueshima 2000
). The finding of a major gene order change within a genus of gastropods, as shown in the present study, adds to a growing body of evidence suggesting that dramatic changes have taken place in the mitochondrial genome during the evolutionary history of this phylum. Why mitochondrial gene rearrangements have been more common within the Mollusca remains an interesting question that can be addressed only through fine-scale reconstructions of the events (e.g., gene duplications, transpositions, inversions, and possibly intramolecular recombination [Lunt and Hyman 1997]
) that have caused these changes. Likewise, understanding why the arrangement of major mitochondrial genes is, in general, so much more stable than the arrangement of tRNA genes in some groups but not others remains a challenging problem.
The mitochondrial gene rearrangement within Dendropoma is also unusual because it has resulted in a physical separation of the two rRNA gene subunits (rrnS and rrnL), which have remained united (usually with an intervening trnV) throughout the evolution of many phyla (Boore 1999
). The juxtaposition of rrnS and rrnL also appears to have been the ancestral arrangement of gastropod molluscs, as inferred from the chiton Katharina (Boore and Brown 1994b
), the cephalopod Loligo (Tomita 1998
), and representatives of seven caenogastropod families (unpublished data). These genes appear to have moved relative to one another, however, within at least two gastropod lineages: within the heterobranch lineage (Yamazaki et al. 1997
; Kurabayashi and Ueshima 2000
), a sister clade to the Caenogastropoda, and also independently within the caenogastropod genus Dendropoma. How this physical separation of rRNA subunits has affected gene regulation mechanisms that promote differential regulation of the synthesis of rRNAs relative to other mitochondrial genes remains to be determined (see Montoya, Gaines, and Attardi 1983
). Nevertheless, such a recent change in gene order offers a particularly tractable system for studying the effects of changes in gene position on mechanisms of gene replication and transcription.
Recent gene rearrangements such as those described here have the potential to reveal considerably more about the mechanics of changes in gene order than ancient events, since long intervening periods of evolution can erase the telltale vestiges of gene duplications and translocations. Such gene remnants, when present, have been instrumental in reconstructing patterns of mitochondrial gene order evolution in many phylogenetic groups (Cantatore et al. 1987
; Arndt and Smith 1998
; Macey et al. 1998
; Dowton and Austin 1999
). Additional sampling of the 20 or more species of Dendropoma should help to determine the full extent of the gene order change within this genus and to reveal the mechanics of this gene rearrangement. More generally, our results indicate that fine-scale sampling within well-resolved phylogenies may uncover additional recent rearrangements, thus enabling us to elucidate the mechanisms underlying gene order change and to determine the frequency of such rearrangements. Our results also suggest that gene orders based on single exemplars may not be representative of the taxa they have been chosen to represent, even at fairly low taxonomic levels. Demonstration of an increased frequency of major gene order rearrangements within lineages, however, will not necessarily indicate that homoplasy is rife within major gene order characters, especially given the number of potential gene order rearrangements. This will likely only be true if such rearrangements are found to be associated with "hot spots" within the mitochondrial genome. Instead, our results demonstrate strong congruence between nucleotide sequence support and gene order support for a clade of Dendropoma (fig. 1A and B
). Consequently, there is hope that once PCR primers spanning gene boundaries are more routinely employed, we may find robust major gene order characters diagnosing clades within orders, families, and genera.
Supplementary Material
Nucleotide sequences have been submitted to GenBank under the accession numbers AF338143–AF338156. The sequence alignment is available on request from the authors or from the journal's website. Voucher specimens are deposited at the Field Museum.
Acknowledgements
We thank Michael G. Hadfield, Isabella Kappner, Richard N. Kilburn, and José Templado for providing us with vermetid specimens. This research was supported by NSF grant number DEB-9509324 to R.B. and T.M.C., and a Tropical Biology Postdoctoral Fellowship to T.A.R. The Smithsonian Marine Station at Ft. Pierce (SMSFP), the Bertha LeBus Charitable Trust, and the Field Museum's Marshall Field Fund supported fieldwork. This is contribution 32 of the program in Tropical Biology at Florida International University and SMSFP contribution number 523.
Footnotes
Richard H. Thomas, Reviewing Editor
1 Keywords: gene order
genomic rearrangement
mitochondrial DNA
rates of molecular evolution
geminate species
Gastropoda 
1 Present address: Department of Palaeontology, Natural History Museum, London, England.
2 Address for correspondence and reprints: Timothy A. Rawlings, Department of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom. t.rawlings{at}nhm.ac.uk
.
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