Contributions to Zoology, 80 (4) 213-230 (2011)

Transformational homology of the tergal setae during postembryonic development in the -Coecobrya group (Collembola: )

Feng Zhang1, 3, Daoyuan Yu1, Guoliang Xu2 1 School of Life Science, Nanjing University, No. 22 Hankou Road, Nanjing 210093, P. R. China 2 Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510160, P. R. China 3 E-mail: [email protected]

Key words: primary homology, larval chaetotaxy, primary setae, s-chaetae

Abstract to develop and unify descriptive methods, particularly in setal nomenclature, which has been performed using The homology concept and its recognition criteria are intro- an evolutionary perspective (Deharveng, 2004). The duced and discussed, with the importance of transformational arrangement of setae (chaetotaxy) in larvae and (primary) homology assessment in phylogenetic analysis em- phasized. We use an ontogenetic approach to explore the setal adults is widely used in descriptive and phylogenetic transformational homology in polychaetotic entomobryid gen- studies of , for example in Collembola, as era (Collembola), where tergal chaetotaxy is usually the most well as Lepidoptera, Coleoptera, Acarina et cetera. informative character for . The postembryonic devel- (Kitching, 1984; Miller, 1991; Archangelsky, 2004; opment of setae on terga of three species in the Sinella-Coeco- Beutel and Leschen, 2005; Solodovnikov, 2007). brya group, , Coecobrya tenebricosa and C. aokii are studied following Szeptycki’s principle. Different However, the problems of chaetotaxic homology of- chaetotaxic patterns of each tergite are homologized and classi- ten affect the reliability of species description and fied for more than 50 species of the two genera. The taxonomi- phylogenetic analysis. cal significance of chaetotaxy of abdomen V, which has been The concept of homology is the fundamental basis rarely studied, is evaluated and affirmed here. The system pre- sented here is a revised and updated from Szeptycki’s system. for comparative and evolutionary biology, as well as phylogenetic systematics. ‘Classical’ homology is a similarity due to historical continuity of information, a Contents feature shared because of descent from a common an- cestral character. Actually, studies employ different Introduction ...... 213 homology concepts in the light of their different inter- Material and methods ...... 215 ests and goals (Brigandt, 2003). Describing and ex- Results ...... 216 plaining the adaptive modification of characters in Postembryonic development of the tergal setae in comparative and evolutionary biology is referred to as S. curviseta, C. tenebricosa and C. aokii ...... 216 Discussion ...... 223 transformational homology. By contrast, taxic homol- Comments on existing systems ...... 223 ogies are features that provide evidence of phyloge- Setal homology ...... 223 netic relationships (taxic homology = synapomorphy) S-chaetotaxy ...... 224 (Patterson, 1982, 1988; Rieppel, 1994; Sluys, 1996). Chaetotaxy of Abd. IV ...... 224 Recognition of homology involves both the estab- Acknowledgements ...... 224 References ...... 224 lishment of a proposition of homology and the subse- Appendix ...... 226 quent affirmation through congruence (Rieppel, 1988), which are evidenced respectively by Remane’s criteria (detailed similarity in position and quality of resem- Introduction blance, see Wiley, 1981), and phylogenetic criteria (con- gruence test). Embryological, ontogenetic and paleon- Taxonomy of Collembola mostly relies on the external tological evidence are the best-known methods used morphology, although limited molecular analyses have for transformational homology assessment, which re- been attempted (D’Haese, 2002; Porco and Deharveng, mains contentious and subjective, yet ultimately cru- 2009). A series of integrated approaches have been used cial in any cladistic analysis (Pimentel and Riggins,

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 214 Zhang et al. – Transformational homology in the Sinella-Coecobrya group

1987; Bryant, 1989; Pogue and Mickevich, 1990; De development of Seira dowlingi (Wray, 1953), Soto- Pinna, 1991; Stevens, 1991; Smith, 1994; Pleijel, 1995; Adames (2008) made some corrections on the homol- Hawkins et al., 1997). ogy of partial setae that was originally proposed by Collembolans are epimetabolic and moult through- Szeptycki (1979). Szeptycki’s hypotheses (1979) on out their lives, where a gradual differentiation occurs setal homology were only based on a few representa- during development. Most setae present in adults are tives, not entirely representing the high diversity and secondary (additional), occurring after first instar. The variability of chaetotaxic patterns that exists in ento- recognition of setal transformational homology of mobryid adults. To expand comparisons of homology adults usually depends on empirical diagnosis, which and avoid the wrong identification of transformational often becomes problematic, because it is difficult to homology in phylogeny, it’s necessary to investigate the discriminate homology of morphologically similar setal transformational homology in more taxa using an setae that are near to each other in a small area, and accurate general method. setae whose morphology varies during postembryonic Jordana and Baquero (2005) also proposed a chaeto- development. The improper determination of transfor- taxic system for Entomobrya and its related genera. mational homology will bring severe confusion in the They studied some species of Entomobrya, Entomo- further phylogenetic analysis. An effective method for bryoides, Homidia and Drepanura, but Sinella and determining the setal transformational homologies Coecobrya were not included. Most setal names of no- needs to be applied to Collembola. Ontogenetic obser- menclature were identical to those of Szeptycki, but vation, which is able to strictly trace the transformation justification for the ‘updated’ reason and changes in and the addition of setae during the postembryonic de- setal nomenclature was not explained, not was the velopment and further establish setal transformational prospect for expanding the system to other genera. homology, could be a much better choice than tradition- The two closely related genera, Sinella and Coeco- al empirical diagnosis in adults. This method primarily brya, both having reduced number of ommatidia, records developmental changes, and indicates that the 4-segmented antennae but with scales and dental spines numbering system and homologies are just hypotheses absent, are widespread and well defined among Ento- and subject to different interpretations. mobryid genera (Deharveng, 1990). Sinella-Coe­ The chaetotaxy on terga, already described for most cobrya group is the second largest group in unscaled entomobryid genera, is a powerful tool in taxonomy Entomobryinae, with more than 90 species reported. and may contribute to the solution of phylogenetic re- Chen and Christiansen (1993, 1997) reviewed the best lationships among genera of Entomobryidae (Yosii, diagnostic characters for the Sinella-Coecobrya group, 1959; Szeptycki, 1979). Setal transformational homol- designating a series of adult chaetotaxic patterns or ogy plays an important role in phylogenetic analyses, groups, which were widely applied during the past fif- and its validity therefore will directly affect the relia- teen years (Chen and Christiansen, 1997; Ma and bility of results. However, the displacement and trans- Chen, 1997; Wang and Christiansen, 2000; Wang et formation, and the secondary addition of tergal setae al., 2002; Chen et al., 2002, 2005; Qu et al., 2007, during postembryonic development results in difficul- 2010). After the examination of plenty of species ty in establishing setal homology in adults. Szeptycki (many undescribed) from East and Southeast Asia, we (1969) was the first one to observe the postembryonic find that the various patterns defined by Chen and development of Entomobryoides myrmecophila (Reu- Christiansen (1993, 1997) can’t be applied to all cases, ter, 1886) in Entomobryidae. Later, Barra (1975) ob- even the conflicts occurring between the known pat- served the same in Pseudosinella decipiens Denis, terns. Because the developmental processes of tergal 1924 and P. impediens Gisin and Da Gama, 1969. setae are quite similar in Entomobryinae particularly Szeptycki (1972, 1979) also made a fundamental con- within genera (Szeptycki, 1979), we study the postem- tribution to the tergal chaetotaxy in Entomobryoidea, bryonic development of the tergal setae of only three by providing a system of nomenclature where he iden- species in detail and further present a general hypothe- tified the homologous setae. sis of setal transformational homologies for the Sinella- However, Szeptycki’s system has not been widely Coecobrya group. It is not possible for us to observe applied in the descriptions or identifications in the past development of all species because some were difficult thirty years, because it is complex and lacks sufficient to culture and we didn’t have enough specimens at assessment of applicability in most entomobryid gen- each stage. In addition, to test the validity of the hy- era and species. After observing the postembryonic potheses and explore the variation in different species,

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 215 we examine the adult chaetotaxy of more than 50 spe- (even longer than macroseta), but it’s much thinner cies of both genera, and point out the flaws of Chen than macroseta. S-chaetae are of two type, microsen- and Christiansen’s classification with more patterns sillum and sensillum, similar terms to those used for newly designated. isotomids. Most primary microsetae in adults are not The complete S-chaetotaxy (chaetotaxy of s-chaetae able to be distinguished from numerous additional mi- / sensilla / setulae / sensory setae / sensorial chaetae / crosetae, although most of them in adults are slightly setae sensuales) has been described in a few species of larger than the additional ones; so only partial primary Sinella and Coecobrya recently by Zhang and Dehar- microsetae could be recognized and labeled in the veng (2009) and Zhang et al. (2009). The use and vari- adult figures. The figures of adult chaetotaxy in C. ability of S-chaetotaxy in both genera are investigated tenebricosa, C. aokii, C. lanna Zhang et al., 2009, C. here for the first time in the Entomobryoidea. similis Deharveng, 1990 and C. tukmeas Zhang et al., The chaetotaxy of Abd. V is usually overlooked in 2009 are redrawn or modified after Zhang et al. the taxonomy of Entomobryoidea and rarely described (2009). although potential availability in this character was Terminology: primary setae-setae occurring at 1st mentioned by Szeptycki (1979). Most setae on this instar; secondary/additional setae-setae occurring af- tergum are usually less differentiated and of great ter 1st instar; s-chaetae-’specialized’ setae of various number. The diversification of Abd. V chaetotaxy in morphology and different from ‘ordinary (common)’ Sinella-Coecobrya group is also illustrated in the pre- setae, often called as sensillar / setulae / sensory setae sent study. / sensorial chaetae / setae sensuales (Deharveng, 2004). Abbreviations: Th.-thoracic segment; Abd.-abdom- inal segment; mac-macroseta(e); mic-microseta(e); Material and methods mes-mesoseta(e); ms-microsensillum/a; s-sensillum/a; Gr.-group. The widespread and typical representatives of the Criteria for homologization of setae: the primary group, Sinella curviseta Brook, 1882 and Coecobrya setae are almost identical in different taxa of Entomo- tenebricosa (Folsom, 1902) were collected from leaf bryinae and easily established in a fixed way. The posi- litter near Nanjing (China) and Paris (France) respec- tion of secondary setae in relation to the primary or tively, and cultured with dry yeast in the laboratory. and other secondary setae, or to those elements whose The third species endemic to Vanuatu (South-west Pa- homology is easier to establish (e.g. bothriotricha, pseu- cific), C. aokii (Yoshii, 1995), was taken from the alco- dopores) is the main criteria. To determine some com- hol material at Museum National d’Histoire Naturelle plicated cases which have several possible hypotheses, (MNHN). Only the specimens of the 1st-3rd instar lar- it’s necessary to find the species with intermediate fea- vae and adults were examined, and their chaetotaxy tures of chaetotaxy. In addition, the displacement of a were discussed and illustrated in the present paper, homologous seta is more probable than its reduction because the homology of most macrosetae in adults, together with the existence of a new one while the po- particularly the primary setae (occurring at 1st instar, sition of setae between two compared species is differ- primary versus secondary/additional), could be ob- ent. The absence of (some) secondary setae is more served before the 4th instar. Specimens were mounted probable than that of primary ones. after clearing in lactic acid under a coverslip in Marc Principle of setal nomenclature: the primary setae André II solution, and were examined using a Leica of each tergum except Abd. IV are designated using DMLB and Nikon E600 microscope. Illustrations the symbol of a letter and a number; the former letter were enhanced with Photoshop CS2. represents the relative position (usually a-anterior, m- The adult chaetotaxy of 57 species of two genera, median, p-posterior) that have been defined in Szep- including 21 unpublished new species are also exam- tycki (1972). The secondary setae are named by a com- ined in the present study (see Appendix). Most mate- bination of the symbol of nearest primary setae and rial examined was from the collections of the MNHN, one or several letters indicating their position in rela- Paris, France and of the School of Life Science, Nan- tion to the former primary ones; a (anterior), p (poste- jing University (NJU), P.R. China. rior), i (internal) and e (external) are used to describe Symbols used in the present paper are shown in Fig. the relative position. For example, p1 represents a pri- 1A. Mesoseta is essentially microseta (common seta) mary seta, p1i a secondary seta located internally to p1, in morphology with larger socket and longer length p1ip a secondary seta posterior to p1i. To avoid repeating

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 216 Zhang et al. – Transformational homology in the Sinella-Coecobrya group letters of setae following each other in the same direc- Coecobrya aokii tion, a series of successive numbers are used to indicate The development of setae in C. aokii is similar to that these setae; e. g., three setae posterior to p1 are desig- in the above two species. S-chaeta ms is internal to s nated respectively as p1p, p1p2 and p1p3 (the first letter as usual. However, the primary setae m2 and p4, and p often deleted in a set of the drawings); sometimes, the secondary setae m4i and m2i are always ciliate mic rows of mac close to the main seta is simply designated (Fig. 2A). as a whole, e.g., m.p1p instead of the above three names. To briefly describe some sets of setae arranged in a Thorax III more or less regular way, these particular setae are con- Sinella curviseta nected to each other with a broken line in the drawings, First instar (Fig. 3A). Eighteen ciliate setae and 2 lat- and designated with the characteristic seta and the eral s occur, with a2-6, m6 and p1-3 as mac and others symbol ‘+’, e.g. set p1+; the largest setae together with mic. Anterior s is internal to m7, another s postero- the largest socket among them usually appear earliest. external to p6. Seta m5 is located anteriorly between a5 and a6, m6 almost aligning with p5 and p6. Second instar (Fig. 3B). Two mac, p2e and m6e, and Results 1 mic, m5i, are added by 2nd instar. Primary setae a1, m5 and p6 change into mac. Seta m6 migrates slightly All figures are located after the references. anteriorly. Third instar (Fig. 3C). The primary setae are un- Postembryonic development of the tergal setae in S. changed at this instar. Nine new setae are added, i.e., curviseta, C. tenebricosa and C. aokii mac a4i, p1p and p2a, mic m1i, a6i, m5p and p5pi, and two setae of unclear homology. Seta m6 migrates fur- Thorax II ther anteriorly. Sinella curviseta Adult (Fig. 3D). A general increase in the number of First instar (Fig. 2B). Totally 19 ciliate setae and 3 s- multiplet mac also occurs during the subsequent in- chaetae occur, with a7, m2, m5, m7 and p4-6 as mic stars. Setae a6i and p5 are transformed into mac. An and others mac. Two s-chaetae (ms and s) are close to additional mac internal to m6 is homologous to m6i. seta m7, ms internal to s; the third s is external to p6. Second instar (Fig. 2C). The primary setae a7 and Coecobrya tenebricosa m2 are transformed into mac. Additional setae a1a, Primary seta a6 is a mic at 1st instar (Fig. 3E) and de- a3a, a4e, a4e2, m4p, m6i, m6p, m7p, p1a, p1p, p2a and velops into a mac at 2nd instar. Mic a6i appears at 2nd p2e appear as mac, m2i, m5a, m5e as mic. The most instar instead of 3rd instar as in S. curviseta (Fig. 3F). postero-lateral 3 additional setae, not labeled as any Mac p2p and a4i also occur at 3rd instar but mic p5pi symbols, are difficult to determine their homology. doesn’t appear at this instar (Fig. 3G). Primary seta p5 Third instar (Fig. 2D). Mac a1p, a4a, a4p, a4e2p, remains as a mic for life. Seta m6 always aligns with a4e2p2, a6ai, a6i and mic a7e are added to the collar. p5 and p6 and never moves anteriorly (Fig. 3H). Additional setae m4i, p1p, p2p and p2ea appear as mac. The primary setae are unchanged. Coecobrya aokii Adult (Fig. 2E). In the subsequent instars and Only a4, a6 and p1-3 are mac at 1st instar, other 13 setae adults, m2i and p2e2 are transformed into mac and a as mic (Fig. 4A). By 2nd instar, primary setae a2, a3 and general increase in the number of mac occurs in most m6 change into mac (Fig. 4B). The adult chaetotaxy multiplets. The position and shape of mic p5-6 and 3 (Fig. 4C) is slightly reduced compared to the above two s-chaetae are unchanged during the postembryonic species; p5, m5i, m6e and m6p never become mac. Seta development. m6 migrates gradually anteriorly during development and at last almost aligns with a6 and p6. Coecobrya tenebricosa The development of most setae in C. tenebricosa is Abdomen I similar to that in S. curviseta. The relative position of Sinella curviseta anterior two s-chaetae is reverse compared to S. curvi- First instar (Fig. 5A). Twelve ciliate setae and 2 s-chae- seta, ms external to s during all instars. Seta m4i rare- tae are primary, with m2-4 as mac. S-chaeta ms is ex- ly changes into a mac in adults (Fig. 1F). ternal to s and a6, s between p5 and p6.

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 217

Second instar (Fig. 5B). No additional setae appear. m3 is mac, others mic. The central s is internal to m3, Third instar (Fig. 5C). A new mac, obviously small- lateral s between pm6 and p6. er than m4 and postero-internal to m4, is designated as Second instar (Fig. 7B). More than 10 additional se- m4p. Another 2 additional mic m2i and m6e appear at tae are added. Primary setae pm6 and p6 change from this instar. mic to mac but am6 remains as mic. Adult (Fig. 5D). Setae m2i and a3 are transformed Third instar (Fig. 7C). A general increase in the into mac. Primary seta a5 remains as a mic for life. number of additional mic occurs. Primary setae are unchanged at this instar. Coecobrya tenebricosa Adult (Fig. 7D). Four mac are present in adults, 1 st At 1 instar, seta a6 is absent and 11 primary setae occur (m3) central and 3 (am6, pm6, p6) lateral. besides s-chaetae; seta m2 is a mic (Fig. 5E). Only 1 additional seta m5i appears and m2 changes from mic Coecobrya tenebricosa nd to mac at 2 instar (Fig. 95F). One mac m4p and 1 mic Primary setae are identical with S. curviseta at 1st in- rd m6e appear at 3 instar as in S. curviseta (Fig. 5G). In star. Seta pm6 changes from mic to mac at 2nd instar; adults, m2i exists as a mac; a mac often present internal the transformation of am6 into a mac occurs at 3rd in- to m4 and antero-internal to m4p is homologous to m4i; star; others never exhibit any changes for life except a seta a3 is observed as a mic for life (Fig. 5H). general increase of mic (Fig. 7E). Coecobrya aokii st Coecobrya aokii Setae a6 and m6 are absent and m2 is also a mic at 1 Primary setae are identical with the above two species instar (Fig. 5I). The additional seta m2i appears and st nd at 1 instar. Seta am6 changes into a mac at 2 instar. m2 remains as a mic at 2nd instar (Fig. 5J). In adults, Setae pm6 and p6 develop into mac in the subsequent m2-4 and m4p are mac, m2i, a3 and a5 mic (Fig. 5K). instars (Fig. 7F). Abdomen II Abdomen IV Sinella curviseta Sinella curviseta First instar (Fig. 6A). There are 15 primary ciliate setae, First instar (Fig. 8A). There are 29 ciliate setae, 2 bo- 2 bothriotricha and 2 s; m3 and m5 are mac, others mic. The central s (‘as’ in Szeptycki’s monograph) is located thriotricha and about 18 (sometimes 17) s. Setae B5 between a2 and a3, the lateral s between p5 and p6. and E3 are mac, others mic. Seta C1 is located in Second instar (Fig. 6B). The mac m3e and 3-4 ad- alignment with B2 and T1. Two of the s-chaetae are ditional mic are added posteriorly to row p. obviously shorter than others, although as long as s on Third instar (Fig. 6C). No obvious changes occur other terga; one is external to T7 and designed as ps by except a few additional mic added. Szeptycki, another is external to B5. Adult (Fig. 6D). Setae a3 external to a2 and m3ep Second instar (Fig. 8B). More than 20 additional se- posterior to m3e are mac in adults. Seta a2 always re- tae are added, with 3-4 mic on the midline. Four pri- mains as mic. mary setae A6, B4, B6, and E4 are transformed into mac. Two secondary mac, designated I and M here, ap- Coecobrya tenebricosa pears postero-external to A3 and between B3 and T2, Primary setae a6, a7 and m7 are absent, others similar respectively. Setae D3, F1 and F3 are apparently larger to those in S. curviseta (Fig. 6E). Setae a2 and a3 are than other mic and develop into mes. A mac between mic for life (Fig. 6F). D2 and F2 appears at this instar; here we consider it to be homologous to E2 in contrast to the position of ‘E2’ Coecobrya aokii in the 1st instar larvae of Seirinae and Lepidocyrtinae. Primary setae a7 and m7 are absent, others similar to Third instar (Fig. 8C). Setae D3 and F1 change into those in C. tenebricosa (Fig. 6G). mac. A4 is rarely transformed into mac. Mac E2p is added, aligning with column E1-2. The sockets of mic Abdomen III D3p, E2a, E4p and F2 are larger than other mic. Sinella curviseta Adult (Fig. 8D). The number and position of mac First instar (Fig. 7A). Fourteen ciliate setae (a few lat- are identical to that at 3rd instar. More mes appear on eral mic of unclear homology not included), 3 (m2, a5, the lateral part with sockets relatively larger but ap- m5) bothriotricha and 2 s appear at this instar. Only parently smaller than those of mac. The long s (the

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 218 Zhang et al. – Transformational homology in the Sinella-Coecobrya group complete arrangement is impossibly observed for their p3a, p4a, p1p and p3pi. In adults, p0 is also present; set loss during specimen preparation) are more than 2 times p4a+ is complete; p4p and p5pe are absent in set p4p+ as long as both ps and another short s external to B5. (Fig. 13B).

Coecobrya tenebricosa Coecobrya aokii At 1st instar (Fig. 9A), about 15 s appear; setae B5 and The chaetotaxy of 1st instar is the same as that in C. E3 are mac. Compared to S. curviseta, B4 moves ante- tenebricosa; seta el is also present (Fig. 13C). Only 2 ro-externally, falling into the column C1-2; B5 and B6 mic, a6a and p6ai, are added at 2nd instar. In adults, p0 also move anteriorly, B5 getting closer to A4; the sec- is also present; set p4a+ is complete; set p4p+ is in- ond short s is postero-external to B5 and internal to complete with only 1 mic p1p present; sets p4a+ and C3. By 2nd instar (Fig. 9B), mac E2 and mic E2p occur p3+ are quite close to each other (Fig. 13D). at the same time; the sockets of mic A6 and B4 are larger than those of other mic. At 3rd instar, A6, B4 and Revision of homology and chaetotaxic patterns in I are transformed into mac; E4 also develops into mes Sinella-Coecobrya group with socket much smaller than that of mac, and into a Homology of some setae in the nomenclature of Szep- mac in the subsequent instars (Fig. 9C). tycki’s system (mainly after figures of Coecobrya hoefti­ ) and the present study are shown in Table 1. Coecobrya aokii The chaetotaxy of 1st instar larvae is similar to that in Thorax II (Fig. 2B) C. tenebricosa except S-chaetotaxy (Fig. 9D); B4 and Compared to Szeptycki’s nomenclature, the main con- B5 are anterior to their normal position; the second flict is the presence or absence of the set a3e+. The short s is between C2 and B5, aligning itself with them. At 2nd instar (Fig. 10A), E2 and E4 changes into mac, with the addition of secondary mac M and mic I. I, A4, A6, B6, F1, E2p and D3 are transformed into mac in Table 1. The nomenclatorial comparison between Szeptycki’s system (mainly after the figures of Coecobrya hoefti) and pre- the subsequent instars (Fig. 10B). The homology of a sent study. seventh dorso-central mac inner to I and rarely present in adults is unclear. Tergite Szeptycki’s system Present study

Abdomen V Th. II a3e a4 a4 a4e Sinella curviseta a4e a4e2 First instar (Fig. 12B). Fourteen ciliate setae and 3 s Abd. I a5 m4 occur, including a mic posterior to pp6 designated as m4 m4p ‘el’ here by the present authors. Setae of row m are a5i m4i larger than others. The inner s is located between a3 Abd. IV A2p A3 A3 I and m3, middle one between p3 and p4, lateral one B3 M internal to p5 (between p4 and p5). E2a E2 Second instar (Fig. 12C). Six additional mic are add- E2 E2p ed. Among them, one antero-external to a6 is designat- Abd. V m5e a6 ed as ‘a6a’, the other antero-external to a5 as ‘a5a’. a6 a6a Third instar (Fig. 12D). Two mic, m3a and p1p, ap- pear. Table 2. The homology of Chen and Christiansen’s groups on Adult (Fig. 12E). All the sets are complete as Szep- Th. II. tycki’s definition. Seta p0 on the midline is present. Group Sets or setae included

Coecobrya tenebricosa I m1+, m2+, m2e st The chaetotaxy of 1 instar is nearly the same as that II a5+, m4+, m4p+ in S. curviseta except that the lateral s is located more III p1i2, p1i, p1, m. p1a anteriorly and between a5 and m5; seta el is also pre- IV m.p1p, m.p1ip, m.p1i2p sent. Three mic, m3a, p6ai and a6a, are added at 2nd V p2+, p3+, p2e+ VI p4+, p2e2+ instar (Fig. 12A). By 3rd instar, 5 mic occur, i.e., m5a,

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 219 chaetotaxy of 2nd instar in the above three species ex- Group I. So far, eight patterns are found respec- hibits the addition of two mac (a4e, a4e2) external to tively with 1-6 mac. Seta m1 is always a mac in all a4, which develops into the sets a4e+ and a4e2+ during patterns, while m2e as a mac only in pattern VIII in S. the subsequent instars. Considering that the mac ante- sp. A. Socket of m1i, if it is a mac, is usually smaller ro-external to a3 apparently belongs the set a3+ and no than others. more secondary mac in relation to it occur for life, this Group II. Four patterns are found (Table 4). Seta m4 mac is homologous to a3a instead of a3e. In addition, is always a mac in all patterns for life, and m4pi is the fact that the sockets of primary mac a3 and a4 is found to be a mac only in pattern IV in S. sp. A. apparently larger than that of mac a3a, a4e and a4e2, Group VI. There are usually 0-2 mac in this area also approves the secondariness of the latter three se- (Table 5). Seta p4p rarely develops into mac in adults. tae. Szeptycki (1979) exhibited the similar process in When only one mac is present in the area of Gr. VI, it the 2nd instar larvae of Orchesella flavescens (Bourlet, is homologous to p4 or p2e2 (Fig. 2B), p4 more exter- 1839), but he used perplexing, wrong names in other nal to p3 than p2e2; while both mac p2e2 and mic p4 species. ‘a4e2, m2e and p2e2’ are newly designated by present, p4 antero-external to p2e2 is easy to be recog- the present authors. nized for its larger socket than those of ordinary mic. Chen and Christiansen (1993) divided the setae on More mac associated to p2e2, all designated as set medial and posterior areas into 6 groups, whose cor- p2e2+ here, are found in S. sp. C (Fig. 2B). If two mac responding homologies are shown in Table 2. Group present in Gr. VI, the homology of the inner one some- III-V are of less taxonomical value because the num- times is difficult to judge; for example, the inner seta in ber of additional setae in these areas is variable from C. tenebricosa, just located internal to p4 and slightly juveniles to adults, even in adult instars. farther from p4 than normal position of p4i, is possibly homologous to p2e2, which is usually considered as p4i (Fig. 1F). Because of the uncertainty of p2e2 in this area, it should be quite careful when giving the Table 3. Macrochaetotaxic patterns of Gr. I on Th. II in adults names. (+ present as mac; - absent or present as mic). The anterior two s-chaetae are close to m7, both in- Pattern m1 M1i m2 m2i m2i2 m2e ternal or both external to m7, or ms internal and s exter- nal to m7. The short ms is usually internal to s except I + - - - - - that in C. tenebricosa. The posterior s is external to p6. II + + - - - - III + - + - - - IV + - + + - - Thorax III (Fig. 4E) V + - + + + - Setal homology coincides well with Szeptycki’s re- VI + + + + - - sults. Primary setae m5, p4 and p5 may remain mic in VII + + + + + - adults; p4 is usually a mic. Primary setae m1, m4, a7 VIII + + + + + + and m7 are always mic for life. The position of two lateral s is stable, respectively internal to m7 and exter- nal to p6. Gr. I-IV were divided by Chen and Chris- tiansen (1993), with their homologies shown in Table 6. The number of setae in Gr. I and II is often variable whatever interspecifically or intraspecifically. Sets a4+ and a5+. Two sets are of great use, usually Table 4. Macrochaetotaxic patterns of Gr. II on Th. II in with 3 patterns present: I, a4, a4i, a5; II, a4, a5; III, a4, adults. a4i, a4i2, a5. The mac a5i is unstable and often absent in adults. Pattern M4 m4p m4i m4pi Group III. The group is of great taxonomical im- I + - - - portance, with five patterns found (Table 7). Seta a6 is II + + - - always a mac in all patterns. Seta m5 is observed as a II + + + - mic only in pattern I in an endemic species C. sp. D IV + + + + (Fig. 4D). Pattern V represents the complete sets m5+ and a6+, which is a most generalized pattern in other Entomobryini and Willowsiini species.

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 220 Zhang et al. – Transformational homology in the Sinella-Coecobrya group

Group IV. Only setae p6 and m6 are always mac in Pattern III, both patterns look to be the same, but ac- adults; their relative position is stable and of taxonom- tually are different. ical value, m6 aligning with p5 and p6 (Fig. 3E-H), or The position of s-chaetae is interspecifically vari- m6 antero-exnternal to p6 (Fig. 4E) or even anterior to able but intraspecifically stable, although the number p6 (Fig. 4D). Setae p5 and m6e always occur but often of s-chaetae (ms and s) on Abd. I is unchangeable. remain as mic. Seta m6i is often absent (Fig. 4D). The internal s usually is located between p5 and p6, ms external to a6 and p6. In some species, both s- Abdomen I (Fig. 5N, Table 8) chaetae move internally, with s closer to p5 and ms The postembryonic development of the above three internal to p6 (Fig. 5M). Both s-chaetae are reverse in species (Fig. 5) demonstrates that the two mac, both S. sp. A (Fig. 5L). external to m3 and socket of posterior one usually smaller than the anterior one, are m4 and m4p instead Abdomen II (Fig. 6H) of a5 and m4 in Szeptycki’s system, with the substitu- The diverse patterns and their stability of dorsal chae- tion of a5i by m4i. Seta a5 never develops into mac totaxy on Abd. II result in its high taxonomical relia- for life in the examined three species, and its distance bility. Our results on homology agree well with Szep- from m4 is much longer than that between m4 and tycki’s system. Setae m3, m3e and m5 are always mac m4p. Primary setae m2-4 are always mac in adults, in both genera. Chen and Christiansen (1993) divided those lateral to them as mic; the sockets of p6, m6 the central area into two parts, M3 arch (m3, m3e+) and m6e are often larger than those of other mic and and inner part. A maximum of 4 mac occurs in M3 easily distinguished; mac a1 and a5 are only present arch; while 3 in arch, m3ep is always transformed into in Pattern VIII in S. sp. A (Fig. 5L). The mac m4i and a mac rather than m3ea. Another difficulty of homol- a5i may be present or absent in adults (Pattern I-III, ogy is the discernment of a2 and a3, the former inter- VIII), so no more separate patterns are recognized nal and the latter external to as (the central s) (Fig. 6D); while they are present (Fig. 5H). Besides 4 patterns while only 1 mac, except m3ei, is present inner to M3 defined by Chen and Christiansen (1993), 4 more pat- arch, it has two possibilities of homology (a2 or a3). terns, V-VIII, are observed in the present study (Ta- The number and position of s-chaetae on Abd. II are ble 8). When m4i absent in Pattern II and present in stable, ms absent.

Table 5. Macrochaetotaxic patterns of Gr. VI on Th. II in adults. Table 7. Macrochaetotaxic patterns of Gr. III on Th. III in adults. Pattern p4 P4i p2e2 Pattern m5 m5i a6 a6i I + - - II + + - I - - + - III - - + II + - + - IV + - + III + - + + IV + + + - V + + + +

Table 6. The homology of Chen and Christiansen’s groups on Table 8. Macrochaetotaxic patterns of Abd. I in adults (* pat- Th. III. tern designated by Chen and Christiansen, 1993).

Group Sets or setae included Pattern a1+ m2i m2 a2 m3 a3 m4 m4p m4i a5 a5i

I a1-3, p1+, p1i+, p1i2+ I* - + + + + + + + +|- - - II a4+, a5+, p2+, p3ip+, p3+, p2e+ II* - + + - + + + + +|- - - III m5+, a6+ III* - + + - + - + + +|- - - IV p5, p6, m6+, m6p+ IV* - - + - + - + + - - - V - - + - + - + - - - - VI - + + - + - + - - - - VII - - + - + + + + - - - VIII + + + + + + + + +|- + +|-

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 221

Abdomen III (Fig. 7G) tween A3 and A4; at 2nd instar, the position of A3 in Primary setae m3 and pm6 are always as mac in adults; relation to all other closer setae would change if A3 is a2, a3, am6 and p6 may develop into mac, other pri- transformed into mac and moves nearby, and thus a mary setae as mic during all the instars. Seta a2 and a3 secondary mic would occur at the original location in- is respectively internal and external to as. stead of mic A3. Compared to the previous idea, an- There are 1+1-4+4 mac possibly present on central other hypothesis, that is the unchanging mic A3 and Abd. III, respectively designated as Pattern I-IV (Fig. additional mac I, performs much better and more rea- 7H) and the latter two patterns rarely present in both sonable here. Similarly, mac M is an additional one genera. rather than primary B3. The sharp displacement of se- Three macrochaetotaxic patterns occur on lateral tae (A3 and B3) in neighbouring two instars (short Abd. III: I, am6, pm6, p6 (Fig. 7F); II, am6, pm6 (Fig. time) seems unimaginable. The further affirmance 7E); III, pm6, p6 (e.g. C. tetrophthalma). An exception could be demonstrated in species having longer dis- occurs in Sinella yosiia Bellinger and Christiansen, tance between A3 and I. 1974, a mac possibly homologous to a7 occurring ex- The sharp movement of B4 and B5 in some species ternal to am6 in the original figure. often brings confusion to the recognition of their ho- Two s are always present on Abd. III, central one mology. In S. curviseta (Fig. 8), mac B4 and B5 don’t (as) between a2 and a3 and lateral one between pm6 obviously move for life, usually located at the general and p6 (Fig. 7A-F). A third s-chaeta (ms) occurs in place as those in most Entomobryini and Willowsiini some species (Fig. 7G), internal to lateral s and ho- species. Compared to S. curviseta, B4 in C. tenebri- mologous to d2 (Snider, 1967) in Lepidocyrtinae. cosa and C. aokii moves antero-externally, resulting in the position beyond bothriotrichum T2; B5 transfers Abdomen IV (Fig. 12A) antero-internally, often beyond A4. In Coecobrya lan- Only primary setae B5 and E3 and secondary seta M na Zhang et al., central pattern in most specimens is are always mac in adults. The development of the above similar to S. curviseta, with slightly forward move- examined three species shows that only primary seta ment of B5; whereas in a few specimens, B4, B5 and B4 may develop into mac between columns A and T on the short s associated with B5 exhibit strongly forward anterior part; seta B3 is always a mic. A mac occurs at movement so that seta B4 is close to the alignment of 2nd instar between D2 and F2 at the position identical B3 and M (Fig. 10C). In a few extreme examples, the with that of E2 in the 1st instar larvae of Seirinae and forward movement of B4 and B5 results in B4 aligning Lepidocyrtinae, so that we consider it homologous to with I and C1. Chen and Christiansen (1993; 1997), E2; at the same instar or subsequent instars, a seta pos- Chen et al. (2002, 2005) and Qu et al. (2007) illus- terior to E2 appears, as a mic (Fig. 9B-C) or as a mac trated many patterns on setal arrangement of central with socket smaller than that of E2 (Fig. 8C-D). There- and lateral parts; homology of these patterns are re- fore, seta ‘B3’, ‘E2a’ and ‘E2’ in Szeptycki’s figures examined, some new patterns or explanations also pro- should be respectively corrected as ‘M’, ‘E2’ and ‘E2p’. vided here. The exceptional case, with numerous mac In Szeptycki’s illustrations, A3 and B3 have more on Abd. IV, is not included in the new patterns for the probabilities to develop into mac than other setae on uncertain homology of some setae. anterior part. The above viewpoint grounds on the fact We concentrate on the changes of primary setae in that primary mic have more probabilities of transfor- central macrochaetotaxic patterns; those patterns with mation into mac than secondary mic in most examined the addition of a few secondary mac are included as species, and thus results that two mac present at 2nd or the variety of primary patterns (Fig. 11). Thirteen ba- 3rd instar on anterior part are considered to be the sic patterns are found in both genera (Table 9). The transformation of mic ‘A3 and B3’. However, we find Pattern III* defined by Chen and Christiansen (1993), that mic A3 and B3 never develop into mac at 2nd and in fact, is identical to their Pattern II*, with the sharply subsequent instars. The relative position particularly forward movement of mac B4 and B5; therefore, the their position in relation to s-chaetae may help to un- Pattern III* of Chen and Christiansen should be can- derstand their homology here. For example, mic A3 in celled. The newly defined Pattern III shown in Table 9 S. curviseta (Fig. 8) at 1st instar locates slightly exter- is displaced by the Pattern II-A* of Chen and Chris- nally to A2 and closer to midline, with 3 neighbouring tiansen, which has mac B6 instead of mic B6 in the s-chaetae around it, anterior one between A2 and B2, Pattern II*. The Pattern IV-A* is homologous to V*, external one posterior to B2, and posterior one be- with the forward movement of B5 in the former. Two

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 222 Zhang et al. – Transformational homology in the Sinella-Coecobrya group

Table 9. Macrochaetotaxic patterns of central Abd. IV in adults Table 10. Macrochaetotaxic patterns of lateral Abd. IV in adults (* pattern designated by Chen and Christiansen, 1993, 1997 and (* pattern originally designated by Chen and Christiansen 1993, Chen et al., 2002, 2005, others newly added by the present au- 1997, others newly added by the present authors). thors). Pattern D3 E2 E2p E3 E4 F1a F1 F2 F3 F3a Pattern I A4 A6 M B4 B5 B6 I* + + + + + + + + + - I* + + + + + + + II* + + + + + - + - + - II* + + + + + + - III* + + + + + - + - - - III(=II-A*) + + + + - + + IV* - + + + + - + - - - IV* + - + + + + - V* - + - + + - + - - - V*(=IV-A*) + + + + - + - VI* + + - + + - - - - - VI* + - + + - + - VII* - + - + + - - - - - VII* - - + + + + - VIII(=IV-A*) + + + + - - + - - - VIII* + - - + - + - IX + + + + - + + - - - IX* - - - + - + - X + + - + + - + + + - X + + - + - + - XI + + + + + - + + + - XI* + - + + - + + XII - + + + + - + + + + XII - - + + - + - XIII + + + + + - - - - - XIII + - + + + + + XIV - + - + ------

varieties of Pattern I are provided here (Fig. 11), I-A Abdomen V (Fig. 13I) with a mac of unclear homology internal to I; I-B, ho- Most setae drawn in Fig. 13I are not mac in adults, but mologous to Patterns X* and X-A* of Chen and Chris- their sockets are obviously larger than those of ordi- tiansen, with a mac Ae7 added. nary additional mic. The setal number is extremely The lateral chaetotaxy is also of great taxonomical variable between species. Five sets are defined by importance, with 14 patterns found (Table 10). Our re- Szeptycki (1979). A seta often present external to a3 in examination of Pattern IV-A* indicated that the origi- adults and named m2a here, is added to the set m2+, nal figure was mistakenly drawn; the revised figure is with its socket often larger than a3. The lateral two designated as Pattern VIII, with the presence of mac setae of the set m5+ are respectively corrected as a6 E3 and mic E4. Six new patterns (IX-XIV) are added; and a6a instead of ‘m5e’ and ‘a6’ named by Szeptycki mac F3a in Pattern XII is discovered for the first time. in the light of the relative distance between m5 and a6. The position of pseudopore is intraspecifically con- A secondary seta antero-external to a5 is also often stant, usually posterior to A4 (Figs 8-9), rarely anterior observed, designated as a5a. Additional seta P0 always to A4 and even beyond bothriotrichum T2 (Fig. 10D). occurs in adults. Seta p4p is often overlooked for its The number and position of s-chaetae are only socket is subequal to those of ordinary mic and obvi- roughly symmetrical between the two sides of the ously smaller than those of other setae of the set p4p+. same specimen (only one specimen of C. similis exhib- The seta el newly added to Szeptycki’s figure is not ites perfect symmetry in our material). Microsensil- observed for the first time in Entomobryidae; Dehar- lum is absent on Abd. IV. Most s on this segment are veng (1979) drawn a seta posterior to ap6 and pp6 in much longer (usually more than 2 times) than those on Lepidocyrtus cf. lanuginosus (Gmelin, 1788) but with- other segments. At least 2 (usually 2) s, are distinctly out any nomenclature. shorter than others and have normal length; one is the The chaetotaxy of Abd. V is usually overlooked in most postero-lateral one (ps), which always occurs ex- the description of entomobryid species except some ternal to T7; another one associated with B5 always figures in Szeptycki’s monograph. The present work occurs external to B5, but its position is more or less exhibits high diversity of chaetotaxy on Abd. V among variable between species and its homology with ‘as’ in Sinella and Coecobrya species. The chaetotaxy of Lepidocyrtinae is unclear (Figs 8-11). The cases with Abd. V provides a new powerful tool for the taxonomy more short s are observed in some New Caledonia spe- of the two genera, possibly most entomobryid genera. cies (Fig. 10D). The only exception is found in S. sp. A, The movement of some sets (sometimes partial setae with more than 40 s of normal length but no obvious of the set) occur in some species. In C. lanna (Fig. 13E), differentiation among them. both sets p4a+ and p4p+ move forward, with setae p3a

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 223 and p4a beyond m2 and m3, and set p4p+ extremely completely unclear. The reconstruction of phylogeny close to p3+. The forward movement of the set p3+ in in Collembola should be based on the most accurate C. similis almost results in the mixture of the sets p4a+ transformational homology assessment. We believe and p3+ (Fig. 13F). that ontogenetic study of postembryonic development The reduction of the sets p4a+ and p4p+ is also of is superior to the study of adults alone (as in Jordana taxonomical importance. In C. sp. E (Fig. 13G), p3a and Baquero’s study) as a method for assessing homol- and p4a of the set p4a+ and nearly the whole set p4p+ ogy of chaetotaxic characters. except p3pi are absent or develop into only ordinary Szeptycki’s system has strict principles and detailed mic, whose sockets are not obviously differentiated. explanations for most mac of each terga, and is there- The complete set p4p+ is absent in C. similis (Fig. fore very useful at species level. The main flaw, as he 13F). Only one seta p1p occurs in set p4p+ in C. aokii wrote in his own book, is that the examined species (Fig. 13D). were too few to cover all the cases. Our present study There are 3-5 (usually 3) s present on Abd. V, ante- focuses on the revision of homology of the tergal setae rior one (as) close to m2 and a3, the middle s internal or in Sinella and Coecobrya and provides more evidence antero-internal to p4, the lateral s anterior to p5 (usually for his hypotheses, and our system is essentially a re- internal to m5). A fourth s antero-internal to p3 appears vised Szeptycki’s system under strict rationale. Because in S. sp. F, while the lateral s moves externally, located of the lack of sufficient information on Entomobrya, externally to m5 (Fig. 13H). Five s are observed in S. sp. we can’t compare Szeptycki’s system and ours to Jor- A, with the sharp modification of each set. dana and Baquero’s system in detail before the postem- bryonic development of Entomobrys spp. is studied. A S-chaetotaxy more comprehensive revision of chaetotaxic homology The S-chaetotaxy has highly intraspecifical stability across Entomobryidae should be made using the on- and interspecifical diversities in number and position. togenetic approach. The formulae of s-chaetae (including both s and ms) on half terga from Th. II to Abd. V are 3, 2/ 2, 2, 2(3), Setal homology ?, 3(4-5), and ms as 1, 0/1, 0, 0(1), 0, 0. The complete s-chaetotaxy of Abd. IV is difficult to observe for the The primary setae are almost identical in all entomo- frequent loss of s-chaetae on Abd. IV during specimen bryid species, even in the adult chaetotaxy (Szeptycki preparation; however, the rough range of s-chaetae 1972). Our study of the Sinella-Coecobrya group also given in the description could provide relevant useful demonstrated this point. Further observation of more information. The variety of s-chaetae on each tergite species in the same group shows strong constancy dur- has been already discussed in the above text. ing postembryonic development. However, the absence of few primary setae in C. tenebricosa and C. aokii exhibits the variation in the 1st instar chaetotaxy of En- Discussion tomobryidae, at least on Abd. I and II. It seems that the classification of genera or species using chaetotaxy of Comments on existing systems 1st instar larvae is almost impossible, although it may be possible at tribal or subfamilial level. The larval Most nomenclature on tergal setae of Jordana and chaetotaxy could be used for the systematics of high Baquero’s (2005) system was identical to Szeptycki’s taxa in Entomobryomorpha, where the phylogeny of original designations; that is, both their system and our most families or subfamilies is still unclear. system were derived from Szeptycki’s system. How- Szeptycki (1979) made an important advance in the ever, they designated the different names without any construction of a nomenclatural system for primary explanation for the modification and didn’t give the and additional setae of representative genera of Ento- reason why their system was better. For example, the mobryoidea (mainly for Entomobryidae). The greatest homologization of a4, a5 and m5 on Th. III has been difficulty in widely applying his system is in the identi- established in Szeptycki (1979), and our present study fication of setal homologies although Szeptycki (1979) in Sinella-Coecobrya also affirms his work, whereas provided some larval chaetotaxy; the displacement and Jordana and Baquero still used ‘a4i, a4 and a5’ with transformation of tergal setae between genera are often m5 absent in their figures. It’s difficult for other col- difficult to trace. Soto-Adames’ (2008) work on Seira lembologists to apply their system, whose rationale is showed some distinct differences from Szeptycki’s

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 224 Zhang et al. – Transformational homology in the Sinella-Coecobrya group work (1979) on this genus. Our study of the Sinella- Acknowledgements Coecobrya group also modified some of Szeptycki’s plan. Although all the mac in adults could be theoreti- The present study was supported by the Ministry of Science and cally named by Szeptycki’s principle, the transforma- Technology of the People’s Republic of China (2006FY120100) and the National Natural Science Foundation of China tional homology of setae occurring at early instars is (30771704, 40801096). easier to establish than that of setae appearing later. Homologization of all mac is impossible to achieve even among closely related species. For this reason, we References focus the homology of the setae that appears at early instars, which are generally considered most impor- Archangelsky M. 2004. Higher-level phylogeny of Hydrophili- tant in taxonomy. Ontogenetic studies of setal homol- nae (Coleoptera: Hydrophilidae) based on larval, pupal and ogy should be expanded across Collembola. adult characters. Systematic Entomology 29: 188-214. Barra JA. 1975. Le développement postembryonnaire de Pseu- dosinella decipiens et P. impediens. Annales de Spéléologie S-chaetotaxy 30: 173-186. Beutel RG, Leschen RAB. 2005. Phylogenetic analysis of The S-chaetotaxy usually remains stable at species Staphyliniformia (Coleoptera) based on characters of larvae level and perhaps has moderate variability in most en- and adults. Systematic Entomology 30: 510-548. tomobryid genera. The limited information in earlier Brigandt I. 2003. Homology in comparative, molecular, and evolutionary developmental biology: The radiation of a con- literature indicates that S-chaetotaxy may be useful in cept. Journal of Experimental Zoology (Molecular and De- the taxonomy of high taxa rather than in species level velopmental Evolution) 299B: 9-17. in Entomobryidae, as is the case in Isotomidae. Brook G. 1882. On a new genus of Collembola (Sinella) allied to Degeeria Nicolet. Journal of the Linnean Society of Lon- Chaetotaxy of Abd. IV don (Zoology) 16: 541-545. Bryant HN. 1989. An evaluation of cladistic and character anal- yses as hypothetico-deductive procedures, and the conse- The chaetotaxy of Abd. IV, which is the most compli- quences for character weighting. Systematic Zoology 38: cated among those of all terga in Entomobryidae with 214-227. the sharp elongation of Abd. IV, is of extreme taxonom- Chen JX, Christiansen KA. 1993. The genus Sinella with spe- ical importance in Sinella and Coecobrya (Chen and cial reference to Sinella s. str. (Collembola: Entomobryidae) of China. Oriental Insects 27: 1-54. Christiansen, 1997). The key revision of setal homolo- Chen JX, Christiansen KA. 1997. Subgenus Coecobrya of the gy on Abd. IV in the present study is I and M, which genus Sinella (Collembola: Entomobryidae) with special occur at 2nd instar and usually develop into mac in reference to the species of China. Annals of the American adults. Our results show that partial primary setae don’t Society of Entomology 90: 1-19. strongly move for life, i.e., they remain located in the Chen JX, Wang F, Christiansen KA. 2002. A new species of the subgenus Coecobrya from Hungary (Collembola: Entomo- same positions as those at early instars. The homology bryidae). Journal of the Kansas Entomological Society 75: of A3 located in medial area in some entomobryid spe- 43-47. cies is doubtful, probably homologous to secondary Chen JX, Leng ZJ, Greenslade P. 2005. Australian species of seta I. A mac antero-internal to bothriotrichum T2 oc- Sinella (Sinella) Brook (Collembola: Entomobryidae). Aus- curs in most entomobryid species, even in Lepidocyrti- tralian Journal of Entomology 44: 15-21. Denis R. 1924. Sur la fauna francaise des Aptérygotes, V. Note nae (‘C1’). In Szeptycki’s monograph (1979), he named préliminaire. Bulletin de la Société Zoologique de France st a seta anterior to T2 at 1 instar as ‘C1’ in two Lepido- 49: 332-386. cyrtinae species with absence of C1 on this figures; D’Haese CA. 2002. Were the first semi-aquatic? A however, his ‘C1’ should be labeled as T1 compared to phylogenetic approach by means of 28S rDNA and optimi- Entomobryinae species; the early work of Barra (1975) zation alignment. Proceedings of the Royal Society B: Bio- logical Sciences 269: 1143-1151. exhibited complete set in P. impediens with the pres- Deharveng L. 1979. Chétotaxie sensillaire et phylogenése chez nd ence of C1, whereas Barra’s figures of 2 instar showed les Collemboles. Travaux du Laboratoire d’Ecobiolologie the seta anterior to T2 is a secondary seta instead of des Arthropodes Edaphiques, Toulouse 1: 1-15. primary seta ‘C1’. The similar nomenclature of anterior Deharveng L. 1990. Fauna of Thai caves. II. New Entomo- setae on Abd. IV in Soto-Adames’ (2008) work is also bryiodea Collembola from Chiang Dao cave, Thailand. Occasional Papers of the Bernice P. Bishop Museum 30: doubtful. The accurate homology needs to be further 279-287. explored in a broader scope and compared between Deharveng L. 2004. Recent advances in Collembola systemat- genera and higher taxa in Entomobryidae. ics. Pedobiologia 48: 415-433.

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 225

De Pinna MCC. 1991. Concepts and tests of homology in the Smith A. 1994. Systematics and the Fossil Record: Document- cladistic paradigm. Cladistics 7: 367-394. ing Evolutionary Pathways. Oxford: Blackwell Scientific. Folsom JW. 1902. Collembola of the grave. Psyche 9: 363-367. Snider RJ. 1967. The Chaetotaxy of North American Lepido- Gisin H, da Gama MM. 1969. Espèces nouvelles de Pseudo­ cyrtus s. str., (Collembola: Entomobryidae). Contributions sinella cavernicoles (Insect: Collembola). Revue Suisse de of the American Entomological Institute 2: 1-28. Zoologie 76: 143-181. Solodovnikov AY. 2007. Larval chaetotaxy of Coleoptera (In- Hawkins JA, Hughes CE, Scotland RW. 1997. Primary homol- secta) as a tool for evolutionary research and systematics: ogy assessment, characters and character states. Cladistics less confusion, more clarity. Journal of Zoological System- 13: 275-283. atics and Evolutionary Research 45: 120-127. Jordana R, Baquero E. 2005. A proposal of characters for taxo- Soto-Adames FN. 2008. Postembryonic development of the nomic identification of Entomobrya species (Collembola, dorsal chaetotaxy in Seira dowlingi (Collembola, Entomo- Entomobryomorpha), with description of a new species. Ab- bryidae); with an analysis of the diagnostic and phylogenetic handlungen und Berichte des Naturkundemuseums Goerlitz significance of primary chaetotaxy in Seira. Zootaxa 1683: 76: 117-134. 1-31. Kitching IJ. 1984. The use of larval chaetotaxy in butterfly sys- Stevens PF. 1991. Character states, morphological variation and tematics, with special reference to the Danaini (Lepido­ phylogenetic analysis: A review. Systematic botany 16: 553- ptera: Nymphalidae). Systematic Entomology 9: 49-61. 583. Ma YT, Chen JX. 1997. A new species of the genus Sinella from Szeptycki A. 1969. Morpho-systematic studies on Collembola. China (Collembola: Entomobryidae). Entomologia Sinica 4: II. Postembryonic development of the chaetotaxy in Ento- 53-55. mobryoides myrmecophila (Reuter, 1886) (Entomobryidae). Miller JS. 1991. Cladistics and classification of the Notodonti- Acta Zoologica Cracoviensia 14: 163-172. dae (Lepidoptera: Noctuoidea) based on larval and adult Szeptycki A. 1972. Morpho-systematic studies on Collembola. morphology. Bulletin of the American Museum of Natural III. Body chaetotaxy in the first instars of several genera of History 204: 1-230. the Entomobryomorpha. Acta Zoologica Cracoviensia 17: Patterson C. 1982. Morphological characters and homology. Pp. 341-372. 21-74 in: Joysey KA, Friday AE, eds, Problems of Phyloge- Szeptycki A. 1979. Morpho-systematic studies on Collembola. netic Reconstruction. London: Academic Press. IV. Chaetotaxy of the Entomobryidae and its phylogenetical Patterson C. 1988. Homology in classical and molecular biolo- significance. Kraków: Polska Akademia Nauk. gy. Molecular Biology and Evolution 5: 603-625. Wang F, Christiansen KA. 2000. A new species of Sinella (Col- Pimentel RA, Riggins R. 1987. The nature of cladistic data. lembola: Entomobryidae) from China. Entomological News Cladistics 3: 201-209. 111: 332-336. Pleijel F. 1995. On character coding for phylogeny reconstruc- Wang F, Chen JX, Christiansen KA. 2002. A new species of the tion. Cladistics 11: 309-315. subgenus Coecobrya (Collembola: Entomobryidae) from Pogue MG, Mickevich MF. 1990. Character definitions and China. Journal of Entomological Science 37: 213-218. character state delineation: The bête-noire of phylogenetic Wiley EO. 1981. Phylogenetics. The Theory and Practice of inference. Cladistics 6: 319-361. Phylogenetic Systematics. New York: John Wiley and Sons. Porco D, Deharveng L. 2009. Phylogeny of Collembola based Wray DL. 1953. Some new species of insects (Col- on cuticular compounds: inherent usefulness and limitation lembola). Nature Notes 1: 1-7. of a character type. Naturwissenschaften 96: 943-954. Yoshii R. 1995. Notes on Collembola of Vanuatu. Acta Zoo- Qu J, Chen JX, Greenslade P. 2007. Australian species of Sinel- logica Asiae Orientalis 3: 43-50. la (Coecobrya) Yosii, 1956 (Collembola: Entomobryidae). Yosii R. 1959. Collembolan fauna of the Cape Province with spe- Journal of Natural History 41: 1301-1311. cial reference to the genus Seira Lubbock. Biological Results Qu JQ, Zhang F, Chen JX. 2010. Two new species of the genus of the Japanese Antarctic Research Expedition 6: 1-24. Sinella Brook, 1882 (Collembola: Entomobryidae) from Zhang F, Deharveng L. 2009. A new cave Sinella species from East China. Journal of Natural History 44: 2535-2541. South China (Collembola: Entomobryidae). Zootaxa 2009: Reuter OM. 1886. For finska faunan nya Podurider.Meddeland - 35-40. en af Societas pro Fauna et Flora Fennica 13: 179-180. Zhang F, Deharveng L, Chen JX. 2009. New species and redi- Rieppel O. 1988. Fundamentals of Comparative Biology. Ber- agnosis of Coecobrya (Collembola: Entomobryidae), with a lin: Birkhauser Verlag. key to the species of the genus. Journal of natural History Rieppel O. 1994. Homology, topology, and typology: The his- 43: 2597-2615. tory of modern debates. Pp. 63-100 in: Hall BK, ed., Homol- ogy: The Hierarchical Basis of Comparative Biology. San Diego: Academic Press. Received: 21 June 2010 Sluys R. 1996. The notion of homology in current comparative Revised and accepted: 9 February 2011 biology. Journal of Zoological Systematics and Evolution- Published online: 26 September 2011 ary Research 34: 145-152. Editor: J.A. Miller

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 226 Zhang et al. – Transformational homology in the Sinella-Coecobrya group

Appendix

Species list and related deposit and collection information (present study).

Coecobrya akiyoshiana Yosii, 1956, Natural History Coecobrya sp. D, MNHN, New Caledonia (Kaala- Museum (Geneva), Japan (Akiyoshi) Gomen) Coecobrya aokii Yoshii, 1995, NJU, Vanuatu Sinella affluensChen and Christiansen, 1993, NJU, (Espiritu Santo, River Saranata) China (Anhui, Chuxian) Coecobrya communis Chen and Christiansen, 1997, Sinella browni Chen and Christiansen, 1993, NJU, NJU, China (Anhui, Chuxian) China (Anhui, Yellow Mountain) Coecobrya guanophila Deharveng, 1990, MNHN, Sinella christianseni Ma and Chen, 1997, NJU, China Thailand (Changwat Chiang Mai: Amphoe Chiang (Anhui, Shitai) Dao, Tham Chiang Dao) Sinella colorata Zhang et al., 2010, NJU, China Coecobrya huangi Chen and Christiansen, 1997, (Guangxi, Huanjiang) NJU, China (Tibet, Zadaqusongbigong) Sinella curviseta Brook, 1882, NJU, China (Jiangsu, Coecobrya indonesiensis Chen and Deharveng, 1997, Nanjing) Museum Zoologicum Bogoriense (Bogor), Indone- Sinella fuyanensis Chen and Christiansen, 1993, sia (Propinsi Sulawesi Selatan, Bone-Watampone) NJU, China (Jiangzi, Ruichang) Coecobrya ishikawai (Yosii, 1956), Natural History Sinella insolens Chen and Christiansen, 1993, NJU, Museum (Geneva), Japan (Kreis Koti, Kusaka China (Jiangsu, Yixing) Mura, Saruta Do) Sinella plebeia Chen and Christiansen, 1993, NJU, Coecobrya lana Zhang, Deharveng and Chen, 2009, China (Anhui, Yellow Mountain) NJU, Thailand (Changwat Chiang Mai: Amphoe Sinella qufuensis Chen and Christiansen, 1993, NJU, Chiang Dao, Doi Chiang Dao) China (Shandong, Qufu) Coecobrya liui Wang, Chen and Christiansen, 2002, Sinella quinocula Chen and Christiansen, 1993, NJU, NJU, China (Qinghai, Laoye Mountain) China (Anhui, Chuxian) Coecobrya magyari Chen, Wang and Christiansen, Sinella samueli Chen, Leng and Greenslade, 2005, 2002, NJU, Hungary (Páter K. u. l., Gödöllö) NJU, Australia (South Australia, Mountain Wood) Coecobrya mulun Zhang et al., 2010, NJU, China Sinella sexoculata (Schött, 1896), Grinnell College, (Guangxi, Huanjiang) USA (California, Berkeley and Alamenda) Coecobrya oligoseta Chen and Christiansen, 1997, Sinella sineocula Chen and Christiansen, 1993, NJU, NJU, China (Jiangsu, Nanjing) China (Jiangsu, Yixing) Coecobrya similis Deharveng, 1990, MNHN, Thai- Sinella termitum Schött, 1917, NJU, Australia land (Changwat Chiang Mai, Amphoe Chiang (Queensland, Ravenshoe) Dao, Ban Tham) Sinella triocula Chen and Christiansen, 1993, NJU, Coecobrya tenebricosa (Folsom, 1902), NJU, France China (Jiangsu, Nanjing) (Paris) Sinella trogla Chen and Christiansen, 1993, NJU, Coecobrya tetrophthalma Denis, 1948, MNHN, China (Guangxi, Guilin) Vietnam (Lam Dong, Dalat, Lang Bian) Sinella umesaoi Yosii, 1940, NJU, China (Jilin, Coecobrya tibetensis Chen and Christiansen, 1997, Changbai Mountain) NJU, China (Tibet, Jilongtuodang) Sinella wui Wang and Christiansen, 2000, NJU, Coecobrya tropicalis Qu, Chen and Greenslade, China (Qinghai, Xining) 2007, NJU, Australia (Learmonth Limestone Sinella whitteni Zhang and Deharveng, 2009, NJU, Lease, Cape Range) China (Guangxi, Yachang Nature Reserve) Coecobrya tukmeas Zhang, Deharveng and Chen, Sinella 9 spp. (sp. A included), MNHN, China 2009, NJU, Cambodia (Kampot, Tuk Meas) (Guangxi and Sichuan) Coecobrya 2 spp., NJU, China (Guangxi) Sinella sp., MNHN, New Caledonia (Lifou island) Coecobrya 5 spp. (sp. E included), MNHN, Vietnam Sinella sp. C, MNHN, New Caledonia (Hienghène, Coecobrya sp., MNHN, Thailand Mont Panié) Coecobrya sp. B, MNHN, Thailand (Chaiyaphum, Sinella sp. F, MNHN, New Caledonia (Bouloupari, Nong Bua Daeng, Tham Keaw) Mont Do)

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 227

Fig. 1. A) Symbols used in the figures. B-E) Chaetotaxy of Th. Fig. 2. A) Adult chaetotaxy of Th. II in C. aokii. B) A diagram II in S. curviseta: B) 1st instar, C) 2nd instar, D) 3rd instar and E) of the final chaetotaxy of Th. II in both genera. adult. F) Adult chaetotaxy of Th. II in C. tenebricosa.

Fig. 3. A-D) Chaetotaxy of Th. III in S. curviseta: A) 1st instar, Fig. 4. A-C) Chaetotaxy of Th. III in C. aokii : A) 1st instar, B) B) 2nd instar, C) 3rd instar and D) adult. E-H) Chaetotaxy of Th. 2nd instar and C) adult. D) Adult chaetotaxy of Th. III in C. sp. III in C. tenebricosa: E) 1st instar, F) 2nd instar, G) 3rd instar and D. E) A diagram of the final chaetotaxy of Th. III in both gen- H) adult. era.

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 228 Zhang et al. – Transformational homology in the Sinella-Coecobrya group

Fig. 5. A-D) Chaetotaxy of Abd. I in S. curviseta: A) 1st instar, Fig. 6. A-D) Chaetotaxy of Abd. II in S. curviseta: A) 1st instar, B) 2nd instar, C) 3rd instar and D) adult. E-H) Chaetotaxy of Abd. B) 2nd instar, C) 3rd instar and D) adult. E-F) Chaetotaxy of Abd. I in C. tenebricosa: E) 1st instar, F) 2nd instar, G) 3rd instar and II in C. tenebricosa: E) 1st instar and F) adult. G) Adult chaeto- H) adult. I-K) Chaetotaxy of Abd. I in C. aokii: I) 1st instar, J) taxy of Abd. II in C. aokii. H) A diagram of the final chaetotaxy 2nd instar and K) adult. L-M) Adult chaetotaxy of Abd. I in L) S. of Abd. II in both genera. I) Macrochaetotaxic patterns of cen- sp. A. and M) C. similis. N) A diagram of the final chaetotaxy of tral Abd. III in both genera. Abd. I in both genera.

Fig. 7. A-D) Chaetotaxy of Abd. III in S. curviseta: A) 1st instar, Fig. 8. Chaetotaxy of Abd. IV in S. curviseta: A) 1st instar, B) 2nd B) 2nd instar, C) 3rd instar and D) adult. E) Adult chaetotaxy of instar, C) 3rd instar and D) adult. Abd. III in C. tenebricosa. F) Adult chaetotaxy of Abd. III in C. aokii. G) A diagram of the final chaetotaxy of Abd. III in both genera.

Downloaded from Brill.com09/29/2021 07:22:16PM via free access Contributions to Zoology, 80 (4) – 2011 229

Fig. 9. A-C) Chaetotaxy of Abd. IV in C. tenebricosa: A) 1st Fig. 10. A Chaetotaxy of Abd. IV in C. aokii: A) 2nd instar and instar, B) 2nd instar and C) adult. D) Primary chaetotaxy of Abd. B) adult. C) Adult chaetotaxy of Abd. IV in C. lanna. D) Adult IV in C. aokii. chaetotaxy of Abd. IV in S. sp. F.

Fig. 11. Macrochaetotaxic patterns of central Abd. IV in both Fig. 12. A) A diagram of the final chaetotaxy of Abd. IV in both genera. genera (few exceptional cases excluded). B-E) Chaetotaxy of Abd. V in S. curviseta: B) 1st instar, C) 2nd instar, D) 3rd instar and E) adult.

Downloaded from Brill.com09/29/2021 07:22:16PM via free access 230 Zhang et al. – Transformational homology in the Sinella-Coecobrya group

Fig. 13. A-B) Chaetotaxy of Abd. V in C. tenebricosa: A) 2nd instar and C) adult. C-D) Chaetotaxy of Abd. V in C. aokii: C) 1st instar and D) adult. E-H) Adult chaetotaxy of Abd. V in E) C. lanna, F) C. similis, G) C. sp. E and H) S. sp. F. I) A diagram of the final chaetotaxy of Abd. V in both genera (the s internal p3 usually absent).

Downloaded from Brill.com09/29/2021 07:22:16PM via free access