Systematics, Historical Biogeography and Ecological Phylogenetics in A

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Zeitschrift/Journal: Denisia

Jahr/Year: 2006

Band/Volume: 0019

Autor(en)/Author(s): Damgaard Jakob

Artikel/Article: Systematics, Historical Biogeography and Ecological Phylogenetics in a clade of water striders 813-822 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Systematics, Historical Biogeography and Ecological Phylogenetics in a clade of water striders1

J. DAMGAARD

Abstract: I hereby review the current knowledge about systematics, historical biogeography and ecological phylogenetics in the three principal northern temperate genera of water striders Limnoporus STÅL 1868, Aquarius SCHELLENBERG 1800 and Gerris FABRICIUS 1794. Most of the discussion is based on comparison of a recently published combined analysis tree involving four genetic markers and a morphological data set with older phylogenetic trees primarily based on manual cladistic optimization of morphological characters.

Key words: DNA-barcodes, Gerrinae, phylogeography, simultaneous analyses.

Introduction nally, water striders show great variation in mating strategies, and morphological and Water striders (Hemiptera-Heteroptera, behavioral adaptations to accomplish or Gerromorpha, Gerridae) are familiar inhab- avoid multiple mating (ANDERSEN 1994, itants of aquatic habitats throughout the 1996; ARNQVIST 1997). The striking diver- Worlds temperate, subtropical, and tropical sity in habitat selection, wing polymorphism regions comprising approximately 640 de- and mating strategies – along with the prac- scribed species in 72 genera (ANDERSEN & tically two dimensional habitat, has made WEIR 2004). Most water striders are found water striders popular objects in studies of in freshwater habitats, such as rivers, behavior, ecology and evolution (SPENCE & streams, lakes and ponds, but a few genera ANDERSEN 1994; ROWE et al. 1994; FAIR- are found in marine – even oceanic – habi- BAIRN et al. 2003; ABE et al. 2004; BERTIN & tats, and still others have become semi-ter- FAIRBAIRN 2005). restrial (ANDERSEN 1982). Being Hemipter- The late Dr. Andersen (1940-2004) ous insects, water striders use their rostrum from the Zoological Museum in Copen- to immobilize and suck out prey, which of- hagen, Denmark, was an expert in extant ten comprises dead or drowning insects and fossil Gerromorpha, and a pioneer in caught in the surface film. Water striders are studies of historical biogeography and eco- particularly variable with respect to wing re- logical phylogenetics (e.g. ANDERSEN 1982, duction, and often display striking patterns 1998; SPENCE & ANDERSEN 1994; ANDERSEN of wing polymorphism (ANDERSEN 1993b, & WEIR 2004). By mapping different traits 1997, 2000). Populations often comprise in question upon a cladogram, he recon- both long-winged (macropterous) and structed ancestral states and inferred the short-winged (brachypterous/micropterous) number and sequence of evolutionary tran- or wingless (apterous) individuals, but the sitions between states. Andersen thereby of- situation may be even more complicated by fered new hypotheses about the evolution of macropterous individuals mutilating their water striders that were not purely specula- wings and/or histolyzing flight muscles, tive but testable, and by dating the events thereby becoming secondarily flightless. Fi- with fossils he furthermore established a

Denisia 19, zugleich Kataloge 1 This paper is dedicated to Dr. Ernst Heiss on the occasion of his 70th birthday and in recognition of his considera- der OÖ. Landesmuseen ble contribution to the study of aradids and their allies. Neue Serie 50 (2006), 813–822

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potheses. As a student of Andersen, I was given the opportunity to participate in studies of the molecular phylogeny of water striders, and after working with the subject for a decade, I find it appropriate to synthe- size the results and outline some of the problems that still prevail about the systematics, ecology, behavior, and distribution of this fascinating group of insects.

Phylogeny Until quite recently, Limnoporus, Aquar- ius and Gerris were treated as subgenera of Gerris, but in a series of papers, ANDERSEN (1975, 1990, 1993b) and ANDERSEN & SPENCE (1992) re-established their generic ranks, and organized their members into presumed monophyletic subgenera and species groups. In his most recent checklist of gerrine water striders, ANDERSEN (1995) listed six species of Limnoporus, 15 species and two subspecies of Aquarius, and three subgenera, 42 species and five subspecies of Gerris. Today, four new species can be added to this assemblage: Aquarius lili POLHEMUS & POLHEMUS 1994, A. remigoides GALLANT & FAIRBAIRN 1996, A. philippinensis ZETTEL & RUIZ 2003, and Gerris kobaishanus LIN- NAVUORI 1998, and there are furthermore indications of several yet undescribed species (ANDERSEN 1990, 1993b; ZIMMER- MANN & SCHOLL 1993; MURAJI 2001; DAMGAARD 2005). Andersen never published a global phylogenetic analysis for the three genera, but his most exhaustive analy- Fig. 1: Phylogenetic relationships among time frame for the evolution of such traits. sis (ANDERSEN 1993b), includes 63 morpho- species, species and subgenera of logical characters scored for two species of Limnoporus, Aquarius and Gerris based on Such hypotheses of course rely heavily on Limnoporus, seven species of Aquarius, and ANDERSEN (1990, 1993b) and ANDERSEN & correct observations and a robust phyloge- 19 species of Gerris. His preferred topology SPENCE (1992). netic reconstruction, and most studies from this analysis (ANDERSEN 1993b: Fig. therefore address a clade comprising the 23), however, was a manual correction of a three principal northern temperate genera, strict consensus of two equally parsimonious Limnoporus STÅL 1868, Aquarius SCHELLEN- trees obtained by a successive approxima- BERG 1800 and Gerris FABRICIUS 1794. By tion weighting of 102 trees. Later he manu- comparing extant and extinct taxa, Ander- ally expanded and corrected this phyloge- sen found that members of the three genera netic reconstruction (e.g. ANDERSEN 1994: exhibited a strong structural stasis in some Fig. 2, 1997: Fig. 4) for inferring evolution- characters, but abundant convergences in ary trends, but the cladograms were never others, probably due to evolutionary and based on computer-based parsimony analy- ecological constraints associated with the ses. In order to summarize Andersen´s hy- life on water surfaces, and realized that mor- potheses of the phylogenetic relationships phological characters alone would not suf- within and between the three genera, the fice for providing robust phylogenetic hy- results from ANDERSEN (1990) and SPENCE

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& ANDERSEN (1992) are therefore inferred onto his preferred tree (Fig. 1). The phylogenetic hypotheses outlined above have been tested repeatedly in simultaneous analyses of genetic and morphological characters (SPERLING et al. 1997; DAMGAARD et al. 2000; DAMGAARD & SPERLING 2001; DAMGAARD & COGNATO 2003), and recently DAMGAARD & COGNA- TO (2005) summarized these studies in a study of 53 species and five subspecies comprising all species of Limnoporus and Aquar- ius and a dense taxon sampling of Gerris including representatives of all subgenera and species groups. The character matrix com- prised 66 morphological characters and DNA sequence data from the mitochondrial protein coding genes for cytochrome c oxi- dase subunit I+II (COI+II 1349 characters); the ribosomal gene encoding the large mitochondrial ribosomal subunit (16SrRNA 426 characters), and the nuclear protein coding gene for elongation factor 1 alpha (EF-1α 515 characters), adding to a total of 2356 characters. A parsimony analysis of this data set gave 8 equally parsimonious trees, and Fig. 2 shows a reduced version of the strict consensus tree (DAMGAARD & COGNATO 2005: Fig. 2). By comparison, the tree based on earlier, morphological studies (Fig. 1) and the combined analysis tree (Fig. 2) give somewhat different conclusions about the phylogenetic relationships within and among the three genera. The most notable differences are (1) Aquarius is monophyletic in Fig. 1 but polyphyletic in Fig. 2 because the A. remigis Morphological versus Fig. 2: Phylogenetic relationships among group is sister group to Gerris, and A. chilen- species, species and subgenera of sis (BERG 1881) is placed unresolved at the molecular characters Limnoporus, Aquarius and Gerris based on basis of the tree; (2) the Limnoporus canalic- DAMGAARD & COGNATO (2005). Despite the more exhaustive taxon sam- ulatus-group from Fig. 1 is paraphyletic in pling in DAMGAARD & COGNATO (2005) Fig. 2 because L. canaliculatus (SAY 1832) is compared to earlier studies, all additional sister species to the L. rufoscutellatus-group species are nested within species groups al- and not to L. esakii (MIYAMOTO 1958); and (3) within Gerris, both the “G. marginatus-” ready represented, and therefore probably and “G. thoracicus-groups” from Fig. 1 are do not contribute much to the overall phy- polyphyletic in Fig. 2, and the G. odonto- logenetic resolution. What matter instead is gaster-group is nested more basal within the addition of molecular characters com- Gerris s.str. prising almost 95 % of the total Partition Branch Support (PBS) (BAKER & DESALLE 1997), which summarizes nodal support from each data partition on the simultaneous analysis tree. Because the morphological

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Fig. 3: Species-area cladogram for Aquarius based on DAMGAARD & COGNATO (2005).

data comprise less than 3 % of the total With the new phylogenetic relationships number of characters, it could look as if the several clades are left without convincing morphological characters are simply morphological synapomorphies. This is most “swamped“ by the molecular data, but when problematic for clades that have been given morphological characters were optimized formal names, such as the genus Aquarius upon the combined analysis tree a posteriori and the subgenus Macrogerris (ANDERSEN (DAMGAARD & COGNATO 2005: Fig. 3) it 1993a) even though both clades may be di- became evident that many synapomorphies agnosed on basis of unique combinations of suggested by earlier studies were still diag- homoplasious characters. ANDERSEN nostic. An inspection of the homoplastic (1993b) used the relative length of the an- characters revealed that several of these tennal segments as his character 3 and gave were poorly defined, or even incorrectly it two states: (1) antennal segments 2+3 scored. As examples are characters in the longer than antennal segment 1 and (2) shape of the male ventral segments 7 and 8 shorter than antennal segment 1. He used in Aquarius which ANDERSEN (1990) used the relatively long segment 1 to diagnose for assigning A. paludum (FABRICIUS 1794) Aquarius, even though MATSUDA (1960) and A. adelaidis (DOHRN 1860) as sister stated that in A. remigis (SAY 1832) and re- species, and A. distanti (HORVÁTH 1899) as lated species, this segment was subequal to sister species to this clade but, as pointed the remaining antennal segments. By using out by DAMGAARD & ZETTEL (2003), these the current, incorrect character states, characters are difficult to score and probably Aquarius is left without synapomorphies but, functionally related. The color of the prono- by giving a third character state for the A. tal disc is another poorly defined character, remigis-group (antennal segments 2+3 sube- which ANDERSEN (1993b) gave only two qual to 1), DAMGAARD & COGNATO (2005) states, but which DAMGAARD & COGNATO gave new diagnostic states for both Aquarius (2005) found should either be ignored or and for the A. remigis-group. Whether diag- broken op into several new states. nostic morphological characters can be

816 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at found for the remaining clades still need to be investigated. Unique nucleotide substitu- tions of a <1kb strand of COI, a.k.a. “DNA- barcodes“, have been used successfully to diagnose clades in other groups of organisms (e.g. HEBERT et al. 2003). Also DAMGAARD & ZETTEL (2003) found that species of the A. paludum-group were monophyletic in their mitochondrial DNA, and that they each could be diagnosed by unique substitu- tions. However, in the much denser popula- tion sampling of the two sibling species Aquarius najas (DEGEER 1773) and A. Fig. 4: Neighbor-joining tree showing cinereus (PUTON 1869), DAMGAARD (2005) genetic distances within and between showed that these two species were not re- members of the Aquarius najas-group after ciprocally monophyletic in their mitochon- DAMGAARD (2005). drial DNA (Fig. 4) Whether this is due to cryptic species, hybridization, incomplete lineage sorting, or something else, still needs to be worked out, but it calls for caution when trying to identify species via a tree- building algorithm, especially when based on a single character system. The conclusion is that molecular characters have provided abundant information, thus leading to new and better supported phylogenetic hypotheses of water strider relationships, and that simultaneous analyses of molecular and morphological characters have offered far better phylogenetic esti- mates than analyses of individual data sets. However, there are major problems also in using molecular data sets. First of all it is very difficult to obtain DNA sequences from museum material that is more than a few years old, unless it has been preserved in strong (96-100 %) ethanol. This is even more so for single copy nuclear genes, such as EF-1α, which only exists in two copies per cell, compared to mitochondrial and/or ribosomal genes, which exists in hundreds or perhaps thousands of copies per cell. Al- though museum material of many species were available due to the earlier studies, it preting the results. It is therefore important has taken long time and involved numerous collaborators all over the World to get the to keep a close collaboration with foremost taxon sampling used in DAMGAARD & COG- the traditional morphologically based tax- NATO (2005), and additional work is needed onomy, in order to evaluate results from mo- in order to obtain fresh material of the Ger- lecular studies. ris species that have not yet been sequenced. Even though molecular systematics is a highly promising discipline, it is still in a premature phase in terms of output, quality, and homologizing of the data, and in inter-

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Taxonomic consequences species, it is evident that the majority of taxa is confined to the Palaearctic Region, Based on the results from DAMGAARD & and that only a few species groups are re- COGNATO (2005) Aquarius obviously needs stricted to the Nearctic Region, or are to be redescribed and restricted to the A. shared between the Palaearctic and Nearc- paludum- and A. conformis-groups and west- tic Regions. However, the relatively species ern Palaearctic members of the A. najas- poor genus Aquarius deserves special atten- group. In such a revision it will be important tion because it – according to the new phy- to determine if A. nebularis (DRAKE & logenetic relationships – is represented by HOTTES 1925) should be synonymized with geographically highly disjunct species in the A. conformis (UHLER 1878), since the two Palaearctic, eastern Nearctic, Afrotropical, species are very much alike both in terms of Oriental, and Australian regions, including morphology and molecules (ANDERSEN several island endemics, such as A. lili from 1990; DAMGAARD et al. 2000), and whether Timor, A. philippinensis from the Philippines, A. najas and A. cinereus have unrecognized and A. paludum amamiensis from Amami- sibling species in the Mediterranea as indi- Oshima and the Ryukyu Islands south of cated by ZIMMERMANN & SCHOLL (1993) Japan (Fig. 3). Only a single fossil, A. lunap- and DAMGAARD (2005). The A. remigis olaensis (LIN 1981) from Miocene Tibet, has group probably needs to be erected to a new been assigned to Aquarius with any certain- generic level and diagnosed on basis of the ty, and was even placed in the A. najas- unique male genitalia and in the relative group on basis of striking similarities (AN- length of antennal segments as compared to DERSEN 1998). If this is true then the present Aquarius and Gerris. Also the four species distribution of the A. najas group in the currently assigned to this clade need to be revised because their taxonomy and exact western Palaearctic region is likely to be re- lictual. The distribution of the three extant distributions are poorly known (ANDERSEN species with A. cinereus in the western 1990; GALLANT & FAIRBAIRN 1996; Mediterranea, A. ventralis (FIEBER 1861) in DAMGAARD unpublished). Finally, the enig- matic “A. chilensis“ shows a mixture of char- the eastern Mediterranea, and A. najas acters that on one side points to the A. na- throughout the western Palaearctic Region jas-group, and on the other side to more (ANDERSEN 1990: Fig. 73) could indicate basal members of Gerrinae as originally dis- speciation in situ, perhaps following isola- cussed by ANDERSEN (1990). Aquarius tion in different refugia during the Pleis- chilensis probably needs to be erected to a tocene glaciations, but this view is contra- new, monotypic genus, but is left unresolved dicted by the deep molecular divergence be- until an investigation of gerrine water strid- tween A. ventralis and A. najas + A. ers have been carried out following the cinereus, which suggests a basal divergence guidelines laid out by MURAJI & TACHIKAWA well before the onset of the glaciations (2000) and DAMGAARD et al. (2005) for the (DAMGAARD 2005) (Fig. 4). The disjunct superfamily Gerroidea. geographical relationship between the eastern Palaearctic A. elongatus (UHLER 1896) and the eastern Nearctic A. conformis/A. Historical biogeography nebularis likewise points to a characteristic Even though Limnoporus, Aquarius and pattern following habitat fragmentation and Gerris are the dominant water strider genera isolation of populations following orogeny in northern temperate regions, only Limno- and climatic changes on the northern porus is strictly Holarctic, while the Gerris Hemisphere during the late Miocene swakopensis-group is found throughout the (DAMGAARD & ZETTEL 2003). However, Afrotropical region (incl. Madagascar), and such palaeoclimatic events probably can not Aquarius was – until the possible exclusion solely be used to explain the distribution of of A. chilensis – considered the only cosmo- the geographically disjunct species in the A. politan genus of water striders (ANDERSEN paludum-group, since sister species relation- 1982, 1990, 1993b, 1995, DAMGAARD & ships here often are found among geograph- COGNATO 2005). When comparing the dis- ically highly disjunct species. POLHEMUS & tribution of subgenera, species groups and POLHEMUS (1994) were the first to suggest

818 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at much older divergences since the newly de- loss of flight ability and maintenance of scribed Timorese A. lili was not sister species wing polymorphism is undoubtedly a conse- to the geographically proximate A. fabricii quence of adaptation through natural selec- ANDERSEN 1990 from northern Australia, tion as first proposed by DARWIN (1872), but instead to the widespread Oriental A. and is probably somehow linked to the adelaidis, even though no geographically in- “flight-oogenesis“ syndrome (JOHNSON termediate populations are known from the 1969) whereby the female divert energy region. DAMGAARD & ZETTEL (2003) and normally used in wing and wing muscle de- DAMGAARD & COGNATO (2005) confirmed velopment to the production of more eggs, the close relationship between A. lili, A. which would increase the female’s fitness adelaidis and the newly described A. philip- more than the advantages associated with pinensis from ancient crater lakes in the the ability to fly. Even though a growing Philippines (ZETTEL & RUIZ 2003), and amount of studies is becoming available, our found that the Afrotropical A. distanti was knowledge of the frequency and determina- sister species to this clade instead of the tion of wing morphs in many species is still trans-Palaearctic A. paludum suggested by highly insufficient. VEPSÄLÄINEN (1974) ANDERSEN (1990). The relatively small ge- suggested that A. najas probably has geneti- netic divergences between A. lili, A. philip- cally determined wing-dimorphism, and pinensis and A. adelaidis seem to contradict long-winged specimens are certainly rare in an ancient diversification of this clade, most northern areas, but may be more com- while the sister group relationship with A. mon in southern latitudes. However, distanti support an ancient vicariance event, AHLROTH et al. (1999) were able to induce probably following the break-up sequence of a high frequency of the long winged morph the southern super-continent Gondwana. from several apparently monomorphic wingless Finnish populations by rearing nymphs Ecological phylogenetics under high temperature and short day- length, thereby simulating more southern ANDERSEN (1993b) hypothesized that latitudes. It was further noticed that popula- the ancestor of the three genera was a wing tions from southern Finland gave a higher dimorphic species, which lived in relatively frequency of the long-winged morph than stable, lentic water bodies with a high de- northern populations, but also that no long- gree of seasonal predictability, and that from winged specimens survived during winter. this ancestral type of ecology, evolution Another particularly well-studied species is went in two directions: (1) species of some the likewise eastern Palaearctic Gerris tho- lineages adapted themselves to lotic habi- racicus, which has two long-winged adult tats, and (2) species of other lineages be- morphs differing in their ability to fly during came adapted to increasingly unstable lentic the reproductive period: “non-flyers“ (with habitats (temporary ponds, water-filled flight muscles histolyzed) that live in the ditches, etc.). Examples of the first category most permanent habitats and “flyers“ (with were the primarily wingless species belong- functional flight muscles) that are able to ing to the Aquarius najas and A. remigis colonize new and temporary habitats during groups, and examples of the second category the breeding season (KAITALA 1988, 1991). were species belonging to the Limnoporus ru- This altogether indicates that the inter- foscutellatus-, Gerris thoracicus-, G. lacustris-, play between genes, development of flight G. marginatus-, and G. odontogaster-groups. muscles and wings, and environment is con- These species are either permanently or sea- siderably more complicated than previously sonally wing-dimorphic or monomorphic believed, and calls for more attention before long-winged, and the most versatile species any general evolutionary trends can be re- were the larger Limnoporus species and Ger- vealed. ris thoracicus SCHUMMEL 1832 Andersen further inferred, that there were two kinds of In water striders, the most common short-winged gerrids, probably as the result mating system is “scramble competition of different mechanisms of morph determi- polygyny (SPENCE & ANDERSEN 1994; “Type nation (genetic versus environmental). The 1 matings“ of ARNQVIST 1997) where the

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male simply lunge at any female within his ics on water striders, and to Dr. Herbert reach, grasps her thorax with his fore legs, Zettel and Dr. Anthony I. Cognato for con- and attempts to insert his phallus into her tributing important ideas in recent joint genital opening. After the copulation prop- projects. Finally I want to thank everybody er has terminated, males usually exhibit who contributed with specimens of water post-copulatory guarding, staying in close striders for my studies, and without whom I contact with the female. Members of the would not have accomplished to get an al- Aquarius remigis-group are unique among most complete taxon-sampling: P. Ahlroth, northern temperate water striders in that G. Arnqvist, C. Askenmo, M. Caterino, M. they stay in genital contact with the female Cherkassova, D. Currie, V. Diaz, H. Dreisig, after the actual mating has taken place. In D.J. Fairbairn, T. Harada, R. Hauser, K. other species the male simply rides the fe- Hayashi, J. Juste, F.E. Klausen, P. Kment, G. males back after copulation, and this post- Koelch, P. Kotlic, D. Kovac, M. Holmen, R. copulatory guarding may last from several Hosseini, M. Itov, O. Karsholt, J.J. Krupa, hours to days in Aquarius najas (ARNQVIST H. Levente, P. Magnien, O. Martin, V. 1997). Because superfluous mating is costly Michelsen, L.G. Nersting, E.S. Nielsen, P. to females (e.g. in terms of increased ener- Nielsen, J. Örnborg, B. Pedersen, B.V. Ped- getic expenditure, reduced mobility, and in- ersen, X. Sá Pinto, D.A. Polhemus, J.T. Pol- creased predation risk), females usually re- hemus, R. Preziosi, A.R. Rasmussen, I. Rib- spond to males by vigorous struggling and era, L. Rowe, R.B. Ruiz, T.J. Simonsen, N. often succeed in dislodging him. Such a sex- Simov, J. Turcinaviciene, C. Villagra, J. Vil- ually antagonistic co-evolution has resulted imova, L.J. Wang & C.M. Yang. This study in the evolution of morphological adapta- was supported by grants from the Danish tions in males that increase their ability to Natural Science Research Council, the grasp females efficiently and distinct mor- Carlsberg Foundation, and the Villum Kann phological adaptations in females that in- Rasmussen Foundation. crease the efficiency with which females dis- lodge males during these struggles (ARN- Zusammenfassung QVIST & ROWE 2002a, b; ROWE & ARN- QVIST 2002). Die Arbeit gibt einen Überblick über Even though the phylogeny of den aktuellen Kenntnisstand der System- Limnoporus, Aquarius and Gerris – and atik, historischen Biogeographie und ökolo- therefore the interpretation of their evolu- gischen Phylogenetik der drei nordtemper- tionary trends – has changed considerably aten Wasserläufergattungen Limnoporus with the inclusion of new molecular data, STÅL 1868, Aquarius SCHELLENBERG 1800 Andersen and others certainly deserves und Gerris FABRICIUS 1794. In der Diskus- credits for synthesizing a broad range of in- sion wird ein aktuell publizierter kom- dividual observations into testable hypothe- binierter Stammbaum aus vier genetischen ses. Whether these hypotheses still hold or Markern und einem morphologischen not will, however, have to await both more Datenset mit älteren, kladistischen Stamm- studies of ecology, ontogeny, adaptation and bäumen morphologischer Merkmale ver- selection, as well as a more robust resolution glichen. of gerrine water strider relationships as men- tioned above.

Acknowledgements I sincerely want to thank the late Dr. Nils Møller Andersen for introducing me to the wonderful world of water striders. I also want to thank Drs. Felix A. H. Sperling, John R. Spence, Masahiko Muraji and Shu- ji Tachikawa for establishing the fundamen- tal framework for doing molecular systemat-

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