- Email: [email protected]
Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides (Acari: Halacaridae: Rhombognathinae)
Zool. Anz. 242 (2004): 293–298 http://www.elsevier-deutschland.de/jcz
Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides (Acari: Halacaridae: Rhombognathinae) Hiroshi ABÉ Biological Laboratory, College of Bioresource Sciences, Nihon University, Fujisawa, Japan Abstract. A morphology-based phylogenetic analysis of the eight species of Rhombognathides (Acari: Halacaridae) demonstrated some evolutionary tendencies of character transformation. In the course of the evolution of Rhombognathides, idiosomal plates increased in size or fused. Simple filiform setae transformed into spiniform or bipectinate setae. The number of tarsal claws, the length of median claw and leg chaetotaxy of telofemora and tibiae were reduced. The fusion or expansion of dorsal plates, transformation from filiform to other setal forms, and reduction of leg setae would have recurrently occurred in halacarid evolution. The claw structure most likely reflects adaptation to specific habitat. Key words. Marine mites, phylogeny, character evolution.
1. INTRODUCTION Character evolution is one of the most fascinating aspects of the evolution of organisms. Up to now there have been several attempts to resolve character transformations of chelicerates through phylogenetic analyses. SHULTZ (1989, 1990) estimated morphological transformations in Arachnida in the light of evolution. WHEELER & HAYASHI (1998) presented phylogenetic implications among chelicerate orders on the basis of molecular data. However, it is sometimes difficult to estimate general evolutionary tendencies on the basis of morphological data in higher categories, especially above familial rank, because of high morphological diversity. Mites are so diverse in form that characterizing each higher taxon is quite difficult. Therefore, I treat species as a primary study unit to embark on a discussion of general evolutionary tendencies. The genus Rhombognathides Viets is one of four marine mite genera in the subfamily Rhombognathinae Viets. The other three genera are Rhombognathus Trouessart, Isobactrus Newell and Metarhombognathus Newell. Intergeneric relationships among these four genera were presented by ABÉ (1998). The monophyly of Rhombognathides was found to be supported by the terminally placed genital foramen in the female, the bacilliform or setiform famulus and the second dor-
sal pore associated with a seta. Recently, a taxonomic revision of Rhombognathides was carried out by ABÉ (2002) on the basis of a cladistic analysis using morphological characters. As a consequence of the analysis, eight distinct species were recognized: Rhombognathides brevipes Bartsch, 1975, R. exoplus (Trouessart, 1901), R. merrimani Newell, 1947, R. mucronatus (Viets, 1927), R. pascens (Lohmann, 1889), R. seahami (Hodge, 1860), R. spinipes (Viets, 1933), and R. trionyx (Trouessart, 1899). The morphological transformation of this mite group, however, has not been examined. My primary aim herein is to inspect evolutionary trends of external morphology within the genus Rhombognathides by using cladistic analysis. Furthermore, I will discuss the evolutionary tendency of each character and provide an evolutionary perspective on character transformation in halacarid mites.
2. MATERIALS AND METHODS 2.1. Morphology of study organisms (Fig.1) The morphological outline employed here is chiefly based on ABÉ (2002). The body is divided into gnathosoma and idiosoma. Four pairs of legs are present. The dorsal plates are well developed and sometimes fused. The ocular plate is fur0044-5231/04/242/04-293 $ 15.00/0
294
H. ABÉ
Fig. 1. Body structures of Rhombognathides. A. Dorsum (female). B. Venter (male). (SEM observation, Scale bars = 100 µm).
nished with three setae and one or two corneae. Nine pairs of dorsal setae in addition to a pair of adanal setae are present. Adjunctive setae are absent. Ventral sclerotization is entire and represented by four distinct plates. The genital and anal plates are completely fused into a genitoanal plate. The female genital opening is terminally placed and guarded by a pair of large cusp-like opercula. The female genitoanal plate is furnished with three pairs of perigenital setae, but lacks subgenital setae. The male usually has three pairs of subgenital setae. The rostrum is furnished with two pairs of rostral setae. The second segment of the palp has one dorsal seta. A solenidion is present on the first and second tarsus, a famulus on the first tarsus. The carpite is rod-shaped. The first and second tarsi each have one spiniform ventral seta. Tarsi I–IV have 2-2-2-2, 3-3-2-2, or 3-3-3-3 claws. Two nymphal stages (proto- and deutonymphs) are known.
unordered, using FITCH parsimony (FITCH 1971). All transformation series were weighted by using a scale weighting option with base weight of one, so that the total influence of each transformation series is the same. Character optimization was executed under two different criteria: accelerated transformation (ACCTRAN) and delayed transformation (DELTRAN) (SWOFFORD & MADDISON 1987). Heuristic search options were used: 1000 replicates of random addition sequences of the taxa with tree-bisection-reconnection (TBR) branch swapping, holding 100 trees at each step, and saving all equally parsimonious trees. This analysis was followed by a successive-approximations approach to character weighting based on the re-scaled consistency index (FARRIS 1969, 1989) to evaluate the strongest transformation series and to choose among equally parsimonious trees (CARPENTER 1988, 1994; EMERSON & HASTINGS 1998).
2.2. Cladistics Morphological data for cladistic analysis were based on ABÉ (2002). The characters of 11 transformation series used in the analysis are listed in Appendix I. The data matrix erected from the discrete morphological characters observed in the transformation series is shown in Appendix II. Multi-characters are treated as polymorphisms. The data matrix was subjected to maximum parsimony analysis using a PAUP 4.0b8a program (SWOFFORD 2002). Based on the cladistic relationships of the four rhombognathine genera (ABÉ 1998), Metarhombognathus was regarded as an outgroup. Multistate transformation series were treated as
3. RESULTS 3.1. Phylogeny (Fig. 2) The first analysis with scaled weighting yielded some equally parsimonious trees, each 21 steps long, with a retention index of 0.8571, re-scaled consistency index of 0.7768, and consistency index of 0.9062. A successiveapproximations approach yielded two equally parsimonious trees (Fig. 2 A, B), each of 21 steps, with a retention index of 0.9787 and consistency index of 0.9792.
Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides
295
Fig. 2. Cladistic relationships among Rhombognathides species. Two equally parsimonious trees (A, B) were obtained. Each character is listed in Appendix I. Solid bars represent single origins; hollow bars represent parallel origins; shaded bars represent underlying synapomorphies.
The present study suggests several monophyletic lineages within the genus. Eight characters plotted onto the cladogram are postulated synapomorphies (Fig. 2). Both character optimization procedures supported the same character distribution on tree A in Fig. 2. These two kinds of optimizations, however, supported different distributions of character 3b on tree B.
3.2. Character evolution Tendencies of character evolution within Rhombognathides are estimated in a phylogenetic context. Despite considerable contradiction, eight characters (1b, 3b, 5a, 5b, 6a, 6b, 7a, and 8a in Fig. 2) consistently defined the species groups recognized by the analysis.
296
H. ABÉ
2. Cornea. 2a. Single cornea –––– 2b. Two corneae The number of corneae on each ocular plate varies from zero to two in halacarid mites. The number varies among genera and even within a genus. Most Rhombognathides species have a single cornea. Addition of a cornea occurred only in the lineages of R. exoplus and R. spinipes (2b in Fig. 2). The presence of two corneae, however, is considered to be plesiomorphy in rhombognathine mites (ABÉ 1998). Therefore, the evolutionary tendency of corneae cannot be estimated here with certainty.
6. Median claw. 6c. Long –––– 6b. Short –––– 6a. Absent A gradual reduction of the median claw is recognized in the present analysis. A tarsus with a long median claw is found in the outgroup Metarhombognathus and is regarded to be plesiomorphic. Only R. mucronatus shares this plesiomorphy. Short median claws are considered to be an underlying synapomorphy of the seven species: R. exoplus, R. seahami, R. pascens, R. trionyx, R. merrimani, R. brevipes, and R. spinipes (6b in Fig. 2). A median claw is absent in three species: R. merrimani, R. brevipes, and R. spinipes (6a in Fig. 2).
3. Interocular seta. 3a. Seta on membrane –––– 3b. Seta on plate The interocular seta is placed either on the membranous cuticle or on the dorsal plate. The presence of interocular seta on the anterior dorsal plate (3b in Fig. 2) is regarded as a synapomorphy in seven species: R. exoplus, R. seahami, R. pascens, R. trionyx, R. merrimani, R. brevipes, and R. spinipes. This character is shared by six species in the case of DELTRAN optimization on tree B. The position of the seta, however, varies depending on developmental condition of the dorsal plates; that is, the seta is located on the plate if dorsal plates are well developed. This character is useful for specific identification, but it is difficult to draw an accurate interpretation in a phylogenetic context.
7. Accessory process. 7a. Endoplanate
4. Basal fossary seta. 4a. Filiform seta –––– 4b. Spiniform seta A spiniform basal fossary seta is regarded as an autapomorphy of R. spinipes (4b in Fig. 2). Morphology of leg setae, i.e. filiform, spiniform, bipectinate, etc., is somewhat variable among the species. The morphology of the basal fossary seta is conservative and it is generally filiform in halacarid mites. Transformation from filiform to spiniform basal fossary setae occurred uniquely in the lineage of R. spinipes.
8. Chaetotaxy of telofemora III–IV. 8b. 3-3 setae –––– 8a. 2-2 setae The setal reduction occurs on the third and fourth telofemora. Plesiomorphy with three setae is reduced to two setae in four species: R. trionyx, R. merrimanni, R. brevipes, and R. spinipes (8a in Fig. 2).
–– –– –
5. Tarsal claw on legs I–II–III–IV. 5c. 3-3-3-3 –––– 5b. 3-3-2-2 –––– 5a. 2-2-2-2 In Rhombognathides evolution, three claws on each tarsus (5c) transformed into two claws (5a) via an intermediate condition (5b) in which there are three claws on the first and second tarsi and two claws on the third and fourth tarsi. Possession of three claws is
–– ––
regarded as a plesiomorphic condition. Tarsi with two claws represents a synapomorphy of three species: R. merrimanni, R. brevipes, and R. spinipes (5a in Fig. 2). The intermediate condition is regarded as an underlying synapomorphy (SAETHER 1979, 1983, 1986) of five species: R. pascens, R. trionyx, R. merrimani, R. brevipes, and R. spinipes (5b in Fig. 2).
–––
1. Dorsal plate. 1a. Four plates –––– 1b. Fused single shield All Rhombognathides species have four dorsal plates, except R. brevipes and R. spinipes that have the plates fused into a single dorsal shield. Fusion of dorsal plates (1b in Fig. 2) uniquely occurred in the common ancestor of R. brevipes and R. spinipes.
7b. Palmate –––– 7c. Absent The tarsal claw is sometimes furnished with an accessory process at its dorsal end. Clear polarity of morphological change could not be obtained in this analysis. An endoplanate accessory process is regarded as an underlying synapomorphy of Rhombognathides (7a in Fig. 2). The outgroup Metarhombognathus has either a palmate accessory process (7b) or a smooth lateral claw (7c). Consequently, these two conditions are regarded to be plesiomorphic under the analytical procedure (7c and 7b in Fig. 2).
9. Chaetotaxy of tibiae III–IV. 9b. 5-5 setae –––– 9a. 4-4 setae A setal reduction is present also on the third and fourth tibiae. This reduction occurs only in R. brevipes and is regarded to be an autapomorphy (9a in Fig. 2). 10. Seta on genu I. 10b. Spiniform seta –––– 10a. Filiform seta –––– –––– 10c. Bipectinate seta Leg setae are filiform, spiniform or bipectinate in shape. Filiform setae have transformed into spiniform
Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides
297
or bipectinate setae during the evolution of Rhombognathides. A spiniform seta on genu I is regarded as an autapomorphy of R. spinipes (10b in Fig. 2). A bipectinate seta has evolved in the lineage of R. mucronatus (10c in Fig. 2).
greatly influenced by habitat (PUGH et al. 1987; BARTSCH 1978). Changes in claw morphology are thought to have occurred in many lineages due to convergence. This means that claw structure may reflect adaptation to particular environments.
11. Chaetotaxy of bipectinate seta on tibia II. 11a. Single bipectinate seta –––– 11b. Two bipectinate setae Most of the Rhombognathides species have a single bipectinate seta on the second tibia. An addition of a bipectinate seta has occurred only in the lineage of R. brevipes (11b in Fig. 2).
Acknowledgements. I thank Dr. I. Bartsch (Forschungsinstitut Senckenberg, Hamburg) for her invaluable suggestions and giving me an opportunity to examine her halacarid collections. I am also indebted to Dr. H. Dastych (Zoologisches Institut und Zoologisches Museum, Universität Hamburg) for lending specimens of Rhombognathides.
REFERENCES 4. DISCUSSION Four sclerotized plates each on dorsum and venter of the body characterize the halacarid mites. According to the character optimization of Rhombognathides, a fused or enlarged dorsal plate is considered to be apomorphy. Such a transformation, however, would have occurred repeatedly during rhombognathine evolution (ABÉ 1998, 2001, 2002). In addition to rhombognathine genera, a fused dorsal plate may also be observed in the halacarid subfamilies Ropohalacarinae Bartsch, Actacarinae Viets and Copidognathinae Bartsch. Fusion or expansion of dorsal plates appears to occur readily during halacarid evolution. Simple filiform leg setae tend to transform into spiniform or bipectinate setae, and the number of bipectinate setae tends to increase in Rhombognathides. The basic morphology of dorsal seta in rhombognathine mites is considered to be filiform (ABÉ 1998). Leg chaetotaxy varies among halacarid mite taxa and developmental stages. Setal reduction occurs on the third and fourth legs in Rhombognathides. ABÉ (1998) performed a cladistic analysis of rhombognathine genera and inferred that the reduction of leg setae occurred in the common ancestor of Isobactrus, Rhombognathides and Metarhombognathus. Because more than one third of halacarid genera display setal reduction on legs, such reduction may be considered a common evolutionary trend in the family. Although claw number tends to be reduced in Rhombognathides, no clear tendency can be observed in the form of the accessory process. It is considered that the Acari primitively have three tarsal claws (EVANS et al. 1961; WOOLLEY 1998). LEE (1984) concluded that the plesiomorphic state of the claw in oribatid mites is possession of two large lateral claws and one small median claw, and a single claw or large three claws are regarded as derived states. Claw number, size and form are highly variable among halacarid genera. Claw morphology varies among species and is
ABÉ, H. (1998): Rhombognathine Mites: taxonomy, phylogeny, and biogeography. iv+219 pp., Hokkaido University Press, Sapporo. ABÉ, H. (2001): Phylogeny and character evolution of the marine mite genus Isobactrus (Acari, Halacaridae). J. Nat. Hist. 35: 617–625. ABÉ, H. (2002): Phylogenetic taxonomy of the marine mite genus Rhombognathides (Acari: Halacaridae: Rhombognathinae). Hydrobiologia 464: 79–88. BARTSCH, I. (1978): Die Krallen der Meeresmilben geben Auskunft über den Lebensraum. Mikrokosmos 67: 197–200. CARPENTER, J. M. (1988): Choosing among multiple equally parsimonious cladograms. Cladistics 4: 291–296. CARPENTER, J. M. (1994): Successive weighting, reliability and evidence. Cladistics 10: 215–220. EMERSON, S. B. & HASTINGS, P. A. (1998): Morphological correlations in evolution: Consequences for phylogenetic analysis. Q. Rev. Biol. 73: 141–162. EVANS, G. O., SHEALS, J. G. & MACFARLANE, D. (1961): The terrestrial Acari of the British Isles: an introduction to their morphology, biology and classification. 219 pp., British Museum (Natural History), London. FARRIS, J. S. (1969): A successive approximations approach to character weighting. Syst. Zool. 18: 374–385. FARRIS, J. S. (1989): The retention index and rescaled consistency index. Cladistics 5: 417–419. FITCH, W. M. (1971): Toward defining the course of evolution: minimum change for a specified tree topology. Syst. Zool. 20: 406–416. LEE, D. C. (1984): A modified classification for oribate mites (Acari: Cryptostigmata). Pp. 241–248 in: GRIFFITHS, D. A. & BOWMAN, C. E. (eds.) Acarology VI. Ellis Horwood, Chichester, England. PUGH, P. J. A., KING, P. E. & FORDY, M. R. (1987): Possible significance of the claw structure in the Rhombognathinae (Halacaridae: Prostigmata: Acari). Acarologia 28: 171–175. SAETHER, O. A. (1979): Underlying synapomorphies and anagenetic analysis. Zool. Scr. 8: 305–312. SAETHER, O. A. (1983): The canalized evolutionary potential: inconsistencies in phylogenetic reasoning. Syst. Zool. 32: 343–359. SAETHER, O. A. (1986): The myth of objectivity – post-Hennigian deviations. Cladistics 2: 1–13.
298
H. ABÉ
SHULTZ, J. W. (1989): Morphology of locomotor appendages in Arachnida: evolutionary trends and phylogenetic implications. Zool. J. Linn. Soc. 97: 1–56. SHULTZ, J. W. (1990): Evolutionary morphology and phylogeny of Arachnida. Cladistics 6: 1–38. SWOFFORD, D. L. (2002): PAUP: phylogenetic analysis using parsimony (and other methods), version 4.0b8a. Sinauer Associates, Sunderland. SWOFFORD, D. L. & MADDISON, W. P. (1987): Reconstructing ancestral character states under Wagner parsimony. Mathl Biosci. 87: 199-229. WHEELER, W. C. & HAYASHI, C. Y. (1998): The phylogeny of the extant chelicerate orders. Cladistics 14: 173–192.
WOOLLEY, T.A. (1998): Acarology: mites and human welfare. xix+484 pp., John Wiley & Sons, New York etc. Author’s address: Hiroshi ABÉ, Biological Laboratory, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, 252-8510 Japan; Tel.: +81-466-84-3723, Fax: +81-466-80-1082, e-mail: [email protected] Received: 15. 10. 2002 Returned for revision: 05. 06. 2003 Accepted: 15. 07. 2003 Corresponding Editor: G. A. BOXSHALL
APPENDIX I.
APPENDIX II.
Transformation series and characters used in the analysis.
Input data matrix.
1. Number of dorsal plates. a. Four plates: Anterior dorsal, right and left ocular and posterior dorsal plates. b. Single plate (anterior dorsal, ocular and posterior dorsal plates are fused). 2. Number of corneae on each ocular plate. a. Ocular plate with single cornea. b. Ocular plate with two corneae. 3. Position of interocular setae. a. Interocular setae are placed on membranous cuticle. b. Interocular setae are placed on dorsal plate. 4. Form of basal fossary setae on each tarsus. a. Filiform seta. b. Spiniform seta. 5. Condition of tarsal claws on legs. a. Two claws on all legs. b. Three claws on legs I and II, two claws on legs III and IV. c. Three claws on all legs. 6. Length of median claw on tarsus I. a. Median claw is absent. b. Median claw is less than or nearly half of the lateral claw. c. Median claw is little shorter than the lateral claw. 7. Form of accessory process. a. Accessory process is broad and endoplanate with many teeth. b. Accessory process is narrow and palmate with a few (-4) teeth. c. Lateral claw is smooth. 8. Leg chaetotaxy of telofemora III–IV. a. Telofemora III–IV with 2-2 setae. b. Telofemora III–IV with 3-3 setae. 9. Leg chaetotaxy of tibiae III–IV. a. Tibiae III–IV with 4-4 setae. b. Tibiae III–IV with 5-5 setae. 10. Leg chaetotaxy of large setae on genu I. a. Genu I without large seta. b. Genu I with a large spiniform seta. c. Genu I with a large bipectinate seta. 11. Leg chaetotaxy of large bipectinate setae on tibia II. a. Tibia II with single bipectinate seta. b. Tibia II with two bipectinate setae.
Taxon Rhombognathides
Transformation series ––––––––––––––––––––––––––––––––––––––––––––––– 1 2 3 4 5 6 7 8 9 10 11
brevipes exoplus merrimani mucronatus pascens seahami spinipes trionyx
b a a a a a b a
a b a a,b a a b a
b ? b a b b b b
a a a a a a b a
a c a c b c a b
a b a c b b a b
b a c a a a c c
a ? a b b b a a
a ? b b b b b b
a ? a c a a b a
b ? a a a a,b a a
Metarhombognathus
a
a,b a
a
c
c
b,c b
b
a
a
Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides (Acari: Halacaridae: Rhombognathinae) Hiroshi ABÉ Biological Laboratory, College of Bioresource Sciences, Nihon University, Fujisawa, Japan Abstract. A morphology-based phylogenetic analysis of the eight species of Rhombognathides (Acari: Halacaridae) demonstrated some evolutionary tendencies of character transformation. In the course of the evolution of Rhombognathides, idiosomal plates increased in size or fused. Simple filiform setae transformed into spiniform or bipectinate setae. The number of tarsal claws, the length of median claw and leg chaetotaxy of telofemora and tibiae were reduced. The fusion or expansion of dorsal plates, transformation from filiform to other setal forms, and reduction of leg setae would have recurrently occurred in halacarid evolution. The claw structure most likely reflects adaptation to specific habitat. Key words. Marine mites, phylogeny, character evolution.
1. INTRODUCTION Character evolution is one of the most fascinating aspects of the evolution of organisms. Up to now there have been several attempts to resolve character transformations of chelicerates through phylogenetic analyses. SHULTZ (1989, 1990) estimated morphological transformations in Arachnida in the light of evolution. WHEELER & HAYASHI (1998) presented phylogenetic implications among chelicerate orders on the basis of molecular data. However, it is sometimes difficult to estimate general evolutionary tendencies on the basis of morphological data in higher categories, especially above familial rank, because of high morphological diversity. Mites are so diverse in form that characterizing each higher taxon is quite difficult. Therefore, I treat species as a primary study unit to embark on a discussion of general evolutionary tendencies. The genus Rhombognathides Viets is one of four marine mite genera in the subfamily Rhombognathinae Viets. The other three genera are Rhombognathus Trouessart, Isobactrus Newell and Metarhombognathus Newell. Intergeneric relationships among these four genera were presented by ABÉ (1998). The monophyly of Rhombognathides was found to be supported by the terminally placed genital foramen in the female, the bacilliform or setiform famulus and the second dor-
sal pore associated with a seta. Recently, a taxonomic revision of Rhombognathides was carried out by ABÉ (2002) on the basis of a cladistic analysis using morphological characters. As a consequence of the analysis, eight distinct species were recognized: Rhombognathides brevipes Bartsch, 1975, R. exoplus (Trouessart, 1901), R. merrimani Newell, 1947, R. mucronatus (Viets, 1927), R. pascens (Lohmann, 1889), R. seahami (Hodge, 1860), R. spinipes (Viets, 1933), and R. trionyx (Trouessart, 1899). The morphological transformation of this mite group, however, has not been examined. My primary aim herein is to inspect evolutionary trends of external morphology within the genus Rhombognathides by using cladistic analysis. Furthermore, I will discuss the evolutionary tendency of each character and provide an evolutionary perspective on character transformation in halacarid mites.
2. MATERIALS AND METHODS 2.1. Morphology of study organisms (Fig.1) The morphological outline employed here is chiefly based on ABÉ (2002). The body is divided into gnathosoma and idiosoma. Four pairs of legs are present. The dorsal plates are well developed and sometimes fused. The ocular plate is fur0044-5231/04/242/04-293 $ 15.00/0
294
H. ABÉ
Fig. 1. Body structures of Rhombognathides. A. Dorsum (female). B. Venter (male). (SEM observation, Scale bars = 100 µm).
nished with three setae and one or two corneae. Nine pairs of dorsal setae in addition to a pair of adanal setae are present. Adjunctive setae are absent. Ventral sclerotization is entire and represented by four distinct plates. The genital and anal plates are completely fused into a genitoanal plate. The female genital opening is terminally placed and guarded by a pair of large cusp-like opercula. The female genitoanal plate is furnished with three pairs of perigenital setae, but lacks subgenital setae. The male usually has three pairs of subgenital setae. The rostrum is furnished with two pairs of rostral setae. The second segment of the palp has one dorsal seta. A solenidion is present on the first and second tarsus, a famulus on the first tarsus. The carpite is rod-shaped. The first and second tarsi each have one spiniform ventral seta. Tarsi I–IV have 2-2-2-2, 3-3-2-2, or 3-3-3-3 claws. Two nymphal stages (proto- and deutonymphs) are known.
unordered, using FITCH parsimony (FITCH 1971). All transformation series were weighted by using a scale weighting option with base weight of one, so that the total influence of each transformation series is the same. Character optimization was executed under two different criteria: accelerated transformation (ACCTRAN) and delayed transformation (DELTRAN) (SWOFFORD & MADDISON 1987). Heuristic search options were used: 1000 replicates of random addition sequences of the taxa with tree-bisection-reconnection (TBR) branch swapping, holding 100 trees at each step, and saving all equally parsimonious trees. This analysis was followed by a successive-approximations approach to character weighting based on the re-scaled consistency index (FARRIS 1969, 1989) to evaluate the strongest transformation series and to choose among equally parsimonious trees (CARPENTER 1988, 1994; EMERSON & HASTINGS 1998).
2.2. Cladistics Morphological data for cladistic analysis were based on ABÉ (2002). The characters of 11 transformation series used in the analysis are listed in Appendix I. The data matrix erected from the discrete morphological characters observed in the transformation series is shown in Appendix II. Multi-characters are treated as polymorphisms. The data matrix was subjected to maximum parsimony analysis using a PAUP 4.0b8a program (SWOFFORD 2002). Based on the cladistic relationships of the four rhombognathine genera (ABÉ 1998), Metarhombognathus was regarded as an outgroup. Multistate transformation series were treated as
3. RESULTS 3.1. Phylogeny (Fig. 2) The first analysis with scaled weighting yielded some equally parsimonious trees, each 21 steps long, with a retention index of 0.8571, re-scaled consistency index of 0.7768, and consistency index of 0.9062. A successiveapproximations approach yielded two equally parsimonious trees (Fig. 2 A, B), each of 21 steps, with a retention index of 0.9787 and consistency index of 0.9792.
Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides
295
Fig. 2. Cladistic relationships among Rhombognathides species. Two equally parsimonious trees (A, B) were obtained. Each character is listed in Appendix I. Solid bars represent single origins; hollow bars represent parallel origins; shaded bars represent underlying synapomorphies.
The present study suggests several monophyletic lineages within the genus. Eight characters plotted onto the cladogram are postulated synapomorphies (Fig. 2). Both character optimization procedures supported the same character distribution on tree A in Fig. 2. These two kinds of optimizations, however, supported different distributions of character 3b on tree B.
3.2. Character evolution Tendencies of character evolution within Rhombognathides are estimated in a phylogenetic context. Despite considerable contradiction, eight characters (1b, 3b, 5a, 5b, 6a, 6b, 7a, and 8a in Fig. 2) consistently defined the species groups recognized by the analysis.
296
H. ABÉ
2. Cornea. 2a. Single cornea –––– 2b. Two corneae The number of corneae on each ocular plate varies from zero to two in halacarid mites. The number varies among genera and even within a genus. Most Rhombognathides species have a single cornea. Addition of a cornea occurred only in the lineages of R. exoplus and R. spinipes (2b in Fig. 2). The presence of two corneae, however, is considered to be plesiomorphy in rhombognathine mites (ABÉ 1998). Therefore, the evolutionary tendency of corneae cannot be estimated here with certainty.
6. Median claw. 6c. Long –––– 6b. Short –––– 6a. Absent A gradual reduction of the median claw is recognized in the present analysis. A tarsus with a long median claw is found in the outgroup Metarhombognathus and is regarded to be plesiomorphic. Only R. mucronatus shares this plesiomorphy. Short median claws are considered to be an underlying synapomorphy of the seven species: R. exoplus, R. seahami, R. pascens, R. trionyx, R. merrimani, R. brevipes, and R. spinipes (6b in Fig. 2). A median claw is absent in three species: R. merrimani, R. brevipes, and R. spinipes (6a in Fig. 2).
3. Interocular seta. 3a. Seta on membrane –––– 3b. Seta on plate The interocular seta is placed either on the membranous cuticle or on the dorsal plate. The presence of interocular seta on the anterior dorsal plate (3b in Fig. 2) is regarded as a synapomorphy in seven species: R. exoplus, R. seahami, R. pascens, R. trionyx, R. merrimani, R. brevipes, and R. spinipes. This character is shared by six species in the case of DELTRAN optimization on tree B. The position of the seta, however, varies depending on developmental condition of the dorsal plates; that is, the seta is located on the plate if dorsal plates are well developed. This character is useful for specific identification, but it is difficult to draw an accurate interpretation in a phylogenetic context.
7. Accessory process. 7a. Endoplanate
4. Basal fossary seta. 4a. Filiform seta –––– 4b. Spiniform seta A spiniform basal fossary seta is regarded as an autapomorphy of R. spinipes (4b in Fig. 2). Morphology of leg setae, i.e. filiform, spiniform, bipectinate, etc., is somewhat variable among the species. The morphology of the basal fossary seta is conservative and it is generally filiform in halacarid mites. Transformation from filiform to spiniform basal fossary setae occurred uniquely in the lineage of R. spinipes.
8. Chaetotaxy of telofemora III–IV. 8b. 3-3 setae –––– 8a. 2-2 setae The setal reduction occurs on the third and fourth telofemora. Plesiomorphy with three setae is reduced to two setae in four species: R. trionyx, R. merrimanni, R. brevipes, and R. spinipes (8a in Fig. 2).
–– –– –
5. Tarsal claw on legs I–II–III–IV. 5c. 3-3-3-3 –––– 5b. 3-3-2-2 –––– 5a. 2-2-2-2 In Rhombognathides evolution, three claws on each tarsus (5c) transformed into two claws (5a) via an intermediate condition (5b) in which there are three claws on the first and second tarsi and two claws on the third and fourth tarsi. Possession of three claws is
–– ––
regarded as a plesiomorphic condition. Tarsi with two claws represents a synapomorphy of three species: R. merrimanni, R. brevipes, and R. spinipes (5a in Fig. 2). The intermediate condition is regarded as an underlying synapomorphy (SAETHER 1979, 1983, 1986) of five species: R. pascens, R. trionyx, R. merrimani, R. brevipes, and R. spinipes (5b in Fig. 2).
–––
1. Dorsal plate. 1a. Four plates –––– 1b. Fused single shield All Rhombognathides species have four dorsal plates, except R. brevipes and R. spinipes that have the plates fused into a single dorsal shield. Fusion of dorsal plates (1b in Fig. 2) uniquely occurred in the common ancestor of R. brevipes and R. spinipes.
7b. Palmate –––– 7c. Absent The tarsal claw is sometimes furnished with an accessory process at its dorsal end. Clear polarity of morphological change could not be obtained in this analysis. An endoplanate accessory process is regarded as an underlying synapomorphy of Rhombognathides (7a in Fig. 2). The outgroup Metarhombognathus has either a palmate accessory process (7b) or a smooth lateral claw (7c). Consequently, these two conditions are regarded to be plesiomorphic under the analytical procedure (7c and 7b in Fig. 2).
9. Chaetotaxy of tibiae III–IV. 9b. 5-5 setae –––– 9a. 4-4 setae A setal reduction is present also on the third and fourth tibiae. This reduction occurs only in R. brevipes and is regarded to be an autapomorphy (9a in Fig. 2). 10. Seta on genu I. 10b. Spiniform seta –––– 10a. Filiform seta –––– –––– 10c. Bipectinate seta Leg setae are filiform, spiniform or bipectinate in shape. Filiform setae have transformed into spiniform
Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides
297
or bipectinate setae during the evolution of Rhombognathides. A spiniform seta on genu I is regarded as an autapomorphy of R. spinipes (10b in Fig. 2). A bipectinate seta has evolved in the lineage of R. mucronatus (10c in Fig. 2).
greatly influenced by habitat (PUGH et al. 1987; BARTSCH 1978). Changes in claw morphology are thought to have occurred in many lineages due to convergence. This means that claw structure may reflect adaptation to particular environments.
11. Chaetotaxy of bipectinate seta on tibia II. 11a. Single bipectinate seta –––– 11b. Two bipectinate setae Most of the Rhombognathides species have a single bipectinate seta on the second tibia. An addition of a bipectinate seta has occurred only in the lineage of R. brevipes (11b in Fig. 2).
Acknowledgements. I thank Dr. I. Bartsch (Forschungsinstitut Senckenberg, Hamburg) for her invaluable suggestions and giving me an opportunity to examine her halacarid collections. I am also indebted to Dr. H. Dastych (Zoologisches Institut und Zoologisches Museum, Universität Hamburg) for lending specimens of Rhombognathides.
REFERENCES 4. DISCUSSION Four sclerotized plates each on dorsum and venter of the body characterize the halacarid mites. According to the character optimization of Rhombognathides, a fused or enlarged dorsal plate is considered to be apomorphy. Such a transformation, however, would have occurred repeatedly during rhombognathine evolution (ABÉ 1998, 2001, 2002). In addition to rhombognathine genera, a fused dorsal plate may also be observed in the halacarid subfamilies Ropohalacarinae Bartsch, Actacarinae Viets and Copidognathinae Bartsch. Fusion or expansion of dorsal plates appears to occur readily during halacarid evolution. Simple filiform leg setae tend to transform into spiniform or bipectinate setae, and the number of bipectinate setae tends to increase in Rhombognathides. The basic morphology of dorsal seta in rhombognathine mites is considered to be filiform (ABÉ 1998). Leg chaetotaxy varies among halacarid mite taxa and developmental stages. Setal reduction occurs on the third and fourth legs in Rhombognathides. ABÉ (1998) performed a cladistic analysis of rhombognathine genera and inferred that the reduction of leg setae occurred in the common ancestor of Isobactrus, Rhombognathides and Metarhombognathus. Because more than one third of halacarid genera display setal reduction on legs, such reduction may be considered a common evolutionary trend in the family. Although claw number tends to be reduced in Rhombognathides, no clear tendency can be observed in the form of the accessory process. It is considered that the Acari primitively have three tarsal claws (EVANS et al. 1961; WOOLLEY 1998). LEE (1984) concluded that the plesiomorphic state of the claw in oribatid mites is possession of two large lateral claws and one small median claw, and a single claw or large three claws are regarded as derived states. Claw number, size and form are highly variable among halacarid genera. Claw morphology varies among species and is
ABÉ, H. (1998): Rhombognathine Mites: taxonomy, phylogeny, and biogeography. iv+219 pp., Hokkaido University Press, Sapporo. ABÉ, H. (2001): Phylogeny and character evolution of the marine mite genus Isobactrus (Acari, Halacaridae). J. Nat. Hist. 35: 617–625. ABÉ, H. (2002): Phylogenetic taxonomy of the marine mite genus Rhombognathides (Acari: Halacaridae: Rhombognathinae). Hydrobiologia 464: 79–88. BARTSCH, I. (1978): Die Krallen der Meeresmilben geben Auskunft über den Lebensraum. Mikrokosmos 67: 197–200. CARPENTER, J. M. (1988): Choosing among multiple equally parsimonious cladograms. Cladistics 4: 291–296. CARPENTER, J. M. (1994): Successive weighting, reliability and evidence. Cladistics 10: 215–220. EMERSON, S. B. & HASTINGS, P. A. (1998): Morphological correlations in evolution: Consequences for phylogenetic analysis. Q. Rev. Biol. 73: 141–162. EVANS, G. O., SHEALS, J. G. & MACFARLANE, D. (1961): The terrestrial Acari of the British Isles: an introduction to their morphology, biology and classification. 219 pp., British Museum (Natural History), London. FARRIS, J. S. (1969): A successive approximations approach to character weighting. Syst. Zool. 18: 374–385. FARRIS, J. S. (1989): The retention index and rescaled consistency index. Cladistics 5: 417–419. FITCH, W. M. (1971): Toward defining the course of evolution: minimum change for a specified tree topology. Syst. Zool. 20: 406–416. LEE, D. C. (1984): A modified classification for oribate mites (Acari: Cryptostigmata). Pp. 241–248 in: GRIFFITHS, D. A. & BOWMAN, C. E. (eds.) Acarology VI. Ellis Horwood, Chichester, England. PUGH, P. J. A., KING, P. E. & FORDY, M. R. (1987): Possible significance of the claw structure in the Rhombognathinae (Halacaridae: Prostigmata: Acari). Acarologia 28: 171–175. SAETHER, O. A. (1979): Underlying synapomorphies and anagenetic analysis. Zool. Scr. 8: 305–312. SAETHER, O. A. (1983): The canalized evolutionary potential: inconsistencies in phylogenetic reasoning. Syst. Zool. 32: 343–359. SAETHER, O. A. (1986): The myth of objectivity – post-Hennigian deviations. Cladistics 2: 1–13.
298
H. ABÉ
SHULTZ, J. W. (1989): Morphology of locomotor appendages in Arachnida: evolutionary trends and phylogenetic implications. Zool. J. Linn. Soc. 97: 1–56. SHULTZ, J. W. (1990): Evolutionary morphology and phylogeny of Arachnida. Cladistics 6: 1–38. SWOFFORD, D. L. (2002): PAUP: phylogenetic analysis using parsimony (and other methods), version 4.0b8a. Sinauer Associates, Sunderland. SWOFFORD, D. L. & MADDISON, W. P. (1987): Reconstructing ancestral character states under Wagner parsimony. Mathl Biosci. 87: 199-229. WHEELER, W. C. & HAYASHI, C. Y. (1998): The phylogeny of the extant chelicerate orders. Cladistics 14: 173–192.
WOOLLEY, T.A. (1998): Acarology: mites and human welfare. xix+484 pp., John Wiley & Sons, New York etc. Author’s address: Hiroshi ABÉ, Biological Laboratory, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, 252-8510 Japan; Tel.: +81-466-84-3723, Fax: +81-466-80-1082, e-mail: [email protected] Received: 15. 10. 2002 Returned for revision: 05. 06. 2003 Accepted: 15. 07. 2003 Corresponding Editor: G. A. BOXSHALL
APPENDIX I.
APPENDIX II.
Transformation series and characters used in the analysis.
Input data matrix.
1. Number of dorsal plates. a. Four plates: Anterior dorsal, right and left ocular and posterior dorsal plates. b. Single plate (anterior dorsal, ocular and posterior dorsal plates are fused). 2. Number of corneae on each ocular plate. a. Ocular plate with single cornea. b. Ocular plate with two corneae. 3. Position of interocular setae. a. Interocular setae are placed on membranous cuticle. b. Interocular setae are placed on dorsal plate. 4. Form of basal fossary setae on each tarsus. a. Filiform seta. b. Spiniform seta. 5. Condition of tarsal claws on legs. a. Two claws on all legs. b. Three claws on legs I and II, two claws on legs III and IV. c. Three claws on all legs. 6. Length of median claw on tarsus I. a. Median claw is absent. b. Median claw is less than or nearly half of the lateral claw. c. Median claw is little shorter than the lateral claw. 7. Form of accessory process. a. Accessory process is broad and endoplanate with many teeth. b. Accessory process is narrow and palmate with a few (-4) teeth. c. Lateral claw is smooth. 8. Leg chaetotaxy of telofemora III–IV. a. Telofemora III–IV with 2-2 setae. b. Telofemora III–IV with 3-3 setae. 9. Leg chaetotaxy of tibiae III–IV. a. Tibiae III–IV with 4-4 setae. b. Tibiae III–IV with 5-5 setae. 10. Leg chaetotaxy of large setae on genu I. a. Genu I without large seta. b. Genu I with a large spiniform seta. c. Genu I with a large bipectinate seta. 11. Leg chaetotaxy of large bipectinate setae on tibia II. a. Tibia II with single bipectinate seta. b. Tibia II with two bipectinate setae.
Taxon Rhombognathides
Transformation series ––––––––––––––––––––––––––––––––––––––––––––––– 1 2 3 4 5 6 7 8 9 10 11
brevipes exoplus merrimani mucronatus pascens seahami spinipes trionyx
b a a a a a b a
a b a a,b a a b a
b ? b a b b b b
a a a a a a b a
a c a c b c a b
a b a c b b a b
b a c a a a c c
a ? a b b b a a
a ? b b b b b b
a ? a c a a b a
b ? a a a a,b a a
Metarhombognathus
a
a,b a
a
c
c
b,c b
b
a
a