© 2007 The Authors Insect Science (2007) 14, 339-350 Development of setal patterns on Hormaphidinae aphids 339 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
Development of setal patterns in embryonic and adult aphids of the Hormaphidinae (Hemiptera: Aphididae) L I - Y U N J I A N G 1, 2, G E - X I A Q I A O 1 a n d G U A N G - X U E Z H A N G 1 1
Institute of Zoology, Chinese Academy of Sciences and 2Graduate University of Chinese Academy of Sciences, Beijing, China Abstract The elementary traits and diversity of embryonic setal patterns of 31 species of 22 genera, in three tribes of Hormaphidinae are studied. The embryonic setal patterns to every species are provided. Based on the parsimony principle and the developmental principle, these patterns are analyzed in each tribe following the terminology of Richards (1965). It is suggested that the setal patterns of abdominal tergites are the most important characters in embryonic and adult setal patterns. In conclusion, neoteny is a phylogenetic trend in the Hormaphidinae. Nipponaphidini and Hormaphidini have more typical neoteny in each genus and more diversity in different types of adult viviparous females than Cerataphidini, by showing more frequent and various protopatterns or mesopatterns. Key words Hemiptera, Hormaphidinae, embryo, adult, setal pattern, development, neoteny DOI 10.1111/j.1744-7917.2007.00160.x
Introduction The subfamily Hormaphidinae belongs to the Aphididae of Hemiptera, and is comprised of three tribes, Cerataphidini, Hormaphidini and Nipponaphidini (Remaudière & Remaudière, 1997). Species of Hormaphidinae are relatively sessile. Most apterous viviparous females are flat, covered with wax powder and have very reduced appendages. Alate viviparous females are of poor activity. The host plants of most species are phylogenetically old. Their primary host plants belong to Hamamelidaceae and Styracaceae, and their secondary host plants are in the Betulaceae, Fagaceae, Lauraceae, Gramineae, and so on. Species of Hormaphidinae are mainly distributed in eastern and southern Asia, but some also in northwestern and northern Europe, and central North America. Of 205 species in 43 genera in the Hormaphidinae worldwide, 75 species of 27 genera are located in China. Aphids are a comparatively large group of Hemiptera
Correspondence: Ge-Xia Qiao, Institute of Zoology, Chinese Academy of Sciences, 25 Besihuanxi Road, Haidian, Beijing 100080, China. Tel: +86 10 6257 1322; fax: +86 10 6256 5689; email:
[email protected]
and their reproduction is so fast that different generations can live in the same large population. The typical mode of reproduction is parthenogenetic vivipary. Thus research on embryos is made easy by finding many mature ones inside adult females. As more aphid species are discovered, especially cryptic species and sister species, we need more characteristics to identify them, and embryos can supply us with new insights in taxonomy and phylogeny. The information based on setal characters, such as shape, length, number and distribution, is very important in morphological taxonomy in aphids. The embryo is an important instar of individual development and the setal patterns of embryos have been used in aphid taxonomy for more than 70 years (Börner, 1930). Since the embryos are very small and contained in the abdomens of females, it was at first difficult to observe and obtain them, and only a few researchers investigated them in the beginning of the 20th century, as did Webster and Phillip (1912). Embryonic setal patterns were first used in aphid taxonomy by Börner (1930). In China, only embryonic setae in the Pemphigidae and the Drepanosiphidae have been studied systematically. The characters of embryos in Tetraneura spp. (Pemphigidae), including the shapes and numbers of setae were described and used in keys of Chinese species (Zhang et al., 1991). Richards
© 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
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Materials and methods
(1965) and later Qiao and Zhang (2003) described the primitive sequence and diversity of setal patterns of the Drepanosiphidae, and discussed the principles concerning the development of setal patterns in its different subfamilies. Noordam (1991) described embryonic setae of aphids in Hormaphidinae of Java in Indonesia, but did not assess their use in taxonomic and phylogenetic study. In this publication we describe and discuss the characters and development of embryonic setal patterns in Hormaphidinae, also including adult setal patterns.
Preparing and observing of embryos Embryos of 31 species in 22 genera were studied, covering all three tribes of Hormaphidinae (Table 1). Embryos were observed within the abdomens of cleared adult viviparous females, or by dissecting abdomens of adult females, if necessary; the embryos were removed from the abdomen and mounted on slides in water, Canada balsam
Table 1 List of species studied in Hormaphidinae. Stages Species
Location Embryo
Cerataphidini Aleurodaphis blumeae van der Goot, 1917 Astegopteryx bambucifoliae (Takahashi, 1921) Astegopteryx bambusae (Buckton, 1893) Astegopteryx minuta (van der Goot, 1917) Cerataphis lataniae (Boisduval, 1867) Ceratoglyphina phragmitidisucta Zhang, 1999 Ceratovacuna lanigera Zehntner, 1897 Ceratovacuna nekoashi (Sasaki, 1910) Chaitoregma tattakana (Takahashi, 1925) Doraphis populi (Maskell, 1898) Glyphinaphis bambusae van der Goot, 1917 Pseudoregma alexanderi (Takahashi, 1924) Pseudoregma bambucicola (Takahashi, 1921) Pseudoregma koshunensis (Takahashi, 1924) Pseudoregma panicola (Takahashi, 1921) Tuberaphis coreana Takahashi, 1933 Tuberaphis cymigalla (Qiao et Zhang, 1998) Tuberaphis viscisucta (Zhang, 1985) Hormaphidini Hamamelistes betulinus (Horvath, 1896) Nipponaphidini Dinipponaphis autumna (Monzen, 1934) Euthoracaphis cinnamoniae (Shinji, 1941) Indonipponaphis fulvicola Sorin, 1979 Metanipponaphis lithocarpicola (Takahashi, 1933) Metanipponaphis silvestrii (Takahashi, 1935) Monzenia globuli (Monzen, 1934) Neonipponaphis shiiae Takahashi, 1962 Neothoracaphis yanonis (Matsumura, 1917) Quadrartus yoshinomiyai Monzen, 1954 Quernaphis chui Zhang, 1992 Reticulaphis distylii fici (Takahashi, 1923) Sinonipponaphis monzeni Takahashi, 1958
China China China China China China China China China China China China China China China Japan China China
+ + + + + + + + + + + + + + + + + +
China
+
Japan Japan Japan China China Japan Japan China Japan China China Japan
+ + + + + + + + + + + +
1st instar 2nd instar 3rd instar nymphs nymphs nymphs
4th instar nymphs
Adult Apt. + + + + + + + + +
Ala.
+ + +
+
+
+
+
+ + + + + + + + +
+
+
+
+
+
+
+ + + +
+ + +
+ +
+
+ +
+ +
+ +
+ + + +
Apt. = apterous viviparous females; Ala. = alate viviparous females.
© 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
Development of setal patterns on Hormaphidinae aphids 341
and chloralphenol. Setal patterns of embryos, every period of nymphs and each type of adults were described and recorded. Observations were carried out under OLYMPUSBHB microscope (Olympus, Tokyo, Japan). Embryonic seta and adult seta used here were only the dorsal body setae. Specimens were collected in China and Japan, and deposited in the Zoological Museum, Institute of Zoology, Chinese Academy of Sciences, Beijing, China. The terminology of Qiao and Zhang (2003) was used here, and the describing methods of setal patterns of Noordam (1991) were followed. Analysis of embryonic setal patterns Elementary mode of embryonic setal patterns was estimated based on principles from parsimony and phylogeny. This means the synapomorphies, those owned by most species or genera and with less diversity, are the most important in this analysis. Embryonic setal patterns express many changes, such as the difference numbers and distributions of dorsal setae on head, thorax and abdomen. In our observations, the setal patterns on abdominal tergites were the lowest diversity and were relatively steady. Therefore, we indicate the differences of setal patterns on the abdomen are the most important divergences in development of embryonic setal patterns, and the embryonic setae pattern with the most popular characters in genera is the elementary mode of embryonic setal patterns in each tribe. This principle is also available in deciding possible directions of development in the embryonic setal patterns. The results support the hypothesis that embryonic setal patterns follow the direction towards reduction of dorsal body setae in Drepanosiphidae (Richards, 1965, Qiao & Zhang, 2003).
Results Analysis of neoteny in adult setal patterns Setal patterns of aphid from embryos to adults mainly concern changes in number and arrangement. Normally, embryos have the least setae and adults have the most. The elementary setal patterns in aphids can be usually divided into three categories by the number of setae, viz. protopattern in embryos and first nymphs, mesopattern in second nymphs and parts of third nymphs, and metapattern in parts of third nymphs, fourth nymphs and adults (Qiao & Zhang, 2003). Neoteny means that adults retain some characters of nymphs, even of embryos in the course of species development. This is represented by adults with protopatterns or mesopatterns in Hormaphidinae.
Embryonic setal patterns of genera in Cerataphidini Embryonic setae of 18 species in Cerataphidini are often fine, acute (Fig. 1e) and rarely thick and strong like in Glyphinaphis (Fig. 1k). Embryonic setal patterns of Cerataphis (Fig. 1e, Qiao & Zhang, 2001) and Tuberaphis (Fig. 1p-r) appear to be the most primordial ones: head vertex with 2 pairs of anterior distal setae and 3 pairs of posterior distal setae (1 pair of spinal, 1 pair of pleural and 1 pair of marginal setae), respectively; pronotum with 1 pair of spinal and 2 pairs of marginal setae, mesonotum and metanotum each with 1 pair of spinal, 1 pair of pleural and 2 pairs of marginal setae, respectively; tergites I－V each with 1 pair of spinal, 1 pair of pleural and 1 pair of marginal setae, respectively; tergites VI － VII each with 1 pair of spinal and 1 pair of marginal setae, and tergite VIII with 1 pair of spinal setae. In several genera, embryonic setal patterns on abdominal tergites are the same as in Cerataphis and Tuberaphis as regards the number and the arrangement, but the patterns are somewhat different on head and thorax. Compared with Cerataphis and Tuberaphis, embryos of Pseudoregma have spinal and/or pleural setae on pronotum, 1 pair added each, and sometimes have a reduction pleural setae on tergite V. (Fig. 1 l-o). In Astegopteryx, embryos also have spinal and pleural setae on pronotum, 1 pair added each, but have pleural setae of head absent (Fig. 1b-d). In embryonic setal patterns of both Aleurodaphis (Fig. 1a) and Ceratovacuna (Fig. 1g, h), pronotum adds 1 pair of spinal setae, while head has only 1 pair of posterior distal setae. In the other genera of Cerataphidini, embryonic setal patterns of abdominal tergites are more or less different from Cerataphis and Tuberaphis. In Chaitoregma (Fig. 1i), tergites I － V add 1 pair of pleural setae each and on the head there are 3 pairs of posterior distal setae (adding 1 pair of spinal and 1 pair of pleural setae and losing marginal setae). Embryos of Doraphis, Ceratoglyphina and Glyphinaphis, have a reduction of pleural setae on the tergites as compared with Cerataphis and Tuberaphis. In Doraphis, embryos have only marginal setae on thoracic nota and no pleural setae on the tergites (Fig. 1j). In Ceratoglyphina, embryos gain 1 pair of posterior distal setae (marginal) on head, but have a reduction of pleural setae on tergites III－V (Fig. 1f). Embryos of Glyphinaphis lose 1 pair of posterior distal setae (spinal) on head and pleural setae on tergites III-V (Fig. 1k). Embryonic setal patterns of genera in Nipponaphidini The genera examined in Nipponaphidini usually have acute, fine or rarely thick embryonic setae. Dinipponaphis (Fig. 2a), Neothoracaphis (Fig. 2h) and Sinonipponaphis
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Fig. 1 Morphological features of embryonic setal patterns of genera in Cerataphidini (a-r) and in Hormaphidini (s). (a) Aleurodaphis blumeae; (b) Astegopteryx bambucifoliae; (c) Astegopteryx bambusae; (d) Astegopteryx minuta; (e) Cerataphis lataniae; (f) Ceratoglyphina phragmitidisucta; (g) Ceratovacuna lanigera; (h) Ceratovacuna nekoashi; (i) Chaitoregma tattakana; (j) Doraphis populi; (k) Glyphinaphis bambusae; (l) Pseudoregma alexanderi; (m) Pseudoregma bambucicola; (n) Pseudoregma koshunensis; (o) Pseudoregma panicola; (p) Tuberaphis coreana; (q) Tuberaphis cymigalla; (r) Tuberaphis viscisucta; (s) Hamamelistes betulinus. © 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
Development of setal patterns on Hormaphidinae aphids 343
(Fig. 2l) have the same embryonic setal patterns, head with 1 pair of anterior distal setae and 3 pairs of posterior distal setae; each thoracic notum with 1 pair of spinal and 2 pairs of marginal setae, respectively; abdominal tergites I－VII each with 1 pair of spinal and 1 pair of marginal setae, respectively; and tergite VIII with 1 pair of spinal setae. Most genera in Nipponaphidini have less spinal setae of abdominal tergites than Dinipponaphis, Neothoracaphis and Sinonipponaphis. In Euthoracaphis (Fig. 2b), embryos lose spinal setae of tergites III－V and VII, and have 1 pair of posterior distal setae (spinal) on head placed forward. In Quadrartus (Fig. 2i), tergites I－VII have no spinal seta, and head has 1 pair of posterior distal setae (pleural) placed forward. The genera, Monzenia (Fig. 2f), Indonipponaphis (Fig. 2c), Metanipponaphis (Fig. 2d, e) and Reticulaphis (Fig. 2k), have no spinal setae on tergites II － VII. Embryos of Indonipponaphis have 1 pair of posterior distal setae (spinal) on head placed forward and spinal setae on pronotum displaced laterally. In Metanipponaphis, embryos have 1 pair of posterior distal setae (pleural) on head placed forward, and sometimes lose 1 pair of marginal setae on mesonotum. In Reticulaphis, embryos add 1 pair of spinal setae on pronotum and have spinal setae on mesonotum displaced to the margin. Only two genera, Neonipponaphis (Fig. 2g) and Quernaphis (Fig. 2j), have the same setal patterns as Dinipponaphis, Neothoracaphis and Sinonipponaphis on abdominal tergites. Embryos of Neonipponaphis have an additional pair of posterior distal setae (spinal) on head and on each of the thoracic nota, and embryos of Quernaphis have pleural setae on head displaced forward, and have lost 1 pair of marginal setae on mesonotum and on metanotum each. Embryonic setal patterns of genera in Hormaphidini This is a small group of aphids. Only one genus, Hamamelistes (Fig. 1s) has been studied. Embryonic setal pattern of H. betulinus is: head with 2 pairs of anterior distal setae, 2 pair of posterior distal setae (spinal, marginal); each thoracic notum with 2 pairs of marginal setae; abdominal tergites I-VII each with 1 pair of marginal setae, only tergites IV－VII each with 1 pair of spinal and 1 pair of marginal setae, and tergite VIII with 1 pair of spinal setae. Neoteny of setal patterns in adults In Cerataphidini, adult apterous viviparous females of eight genera, adult alate viviparous females of one genus and both morphs of one genus were observed. Apterous adults of four genera, Cerataphis,
Ceratoglyphina, Chaitoregma and Pseudoregma, have obvious metapatterns as setae of each tergite are much more numerous than in the embryos. Apterous viviparous females of Astegopteryx and Tuberaphis show mesopatterns. In apterous viviparous females of Aleurodaphis, setal patterns are gradually modified as head and thoracic nota are mesopatterns, and abdominal tergites are protopatterns. In Glyphinaphis, the shape of the seta is thick and strong from embryos to adults, and adult setal patterns almost remain the same as in embryos; having the only typical neotenic setal pattern in the tribe. In apterous and alate viviparous females of Ceratovacuna, head and thoracic nota are metapatterns, and abdominal tergites are mesopatterns, having a few more pleural and marginal setae than the embryos. Alate viviparous females of Doraphis show metapatterns. In Nipponaphidini, apterous viviparous females of four genera, alate viviparous females of four genera and both types in three genera were studied. Apterous viviparous females have simplified setal patterns in both Neothoracaphis and Sinonipponaphis in form of protopatterns. However, the other genera display different drgrees of complex setal patterns. In adults of Indonipponaphis and Metanipponaphis, head and abdominal tergites are protopatterns, and thoracic nota are mesopatterns. In adults of Reticulaphis, head and thoracic nota are mesopatterns, and abdominal tergites are metapatterns. Adults of Neonipponaphis and Euthoracaphis both have metapatterns on head and thoracic nota, but the former genus has protopatterns on abdominal tergites I, V －VII and metapatterns on tergites II－IV, VIII, the latter genus metapatterns on tergite I and mesopatterns on tergites II-VIII. Adult alate viviparous females in Euthoracaphis show protopatterns, in Sinonipponaphis mesopatterns and Quadrartus metapatterns. Neothoracaphis has protopatterns on head and thoracic nota, and mesopatterns on abdominal tergites. Quernaphis, on the contrary, show mesopatterns on head and thoracic nota, and protopatterns on abdominal tergites. In adults of Monzenia, head and abdominal tergites I－VII are mesopatterns, and thoracic nota and tergite VIII are metapatterns. In adults of Dinipponaphis, head, thoracic nota and abdominal tergites I- VII are mesopatterns, and tergite VIII is a metapattern. In Hamamelistes of Hormaphidini, adult apterous viviparous females show protopatterns and adult alate viviparous females mesopatterns. Setal patterns of different types of viviparous females in the same specie In the five genera including both adult apterous and alate
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Fig. 2 Morphological features of embryonic setal patterns of genera in Nipponaphidini (a-1). (a) Dinipponaphis autumna; (b) Euthoracaphis cinnamoniae; (c) Indonipponaphis fulvicola; (d) Metanipponaphis lithocarpicola; (e) Metanipponaphis silvestrii; (f) Monzenia globuli; (g) Neonipponaphis shiiae; (h) Neothoracaphis yanonis; (i) Quadrartus yoshinomiyai; (j) Quernaphis chui; (k) Reticulaphis distylii fici; (l) Sinonipponaphis monzeni. © 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
Development of setal patterns on Hormaphidinae aphids 345
viviparous females, only setal patterns of Ceratovacuna in Cerataphidini are uniform and the others differ more or less in the two morphs. In Hamamelistes, adult apterous viviparous females have rather more setae than alate viviparous females, the former being mesopatterns and the latter protopatterns. However, in adults of Nipponaphidini, most apterous viviparous females have fewer dorsal setae than alate viviparous females, except for Euthoracaphis. In Sinonipponaphis, apterous viviparous females show protopatterns and alate viviparous females have mesopatterns. In Neothoracaphis, apterous viviparous females have the same patterns in common with alate viviparous females on head and thoracic nota, but show protopatterns instead of mesopatterns on abdominal tergites. In Euthoracaphis, alate viviparous females show protopatterns, but the apterous viviparous females metapatterns on head and thoracic nota and a mixture of metapatterns and mesopatterns on abdominal tergites.
Discussion Elementary mode of setal patterns in Hormaphidinae Following our principle of parsimony, the typical embryonic setae pattern of Cerataphidini is head with 5 pairs of setae; pronotum with 1 pair of spinal and 2 pairs of marginal setae, mesonotum and metanotum each with 1 pair of spinal, 1 pair of pleural and 2 pairs of marginal setae, respectively; abdominal tergites I－V each with 1 pair of spinal, 1 pair of pleural and 1 pair of marginal setae, respectively; tergites VI-VII each with 1 pair of spinal and 1 pair of marginal setae, and tergite VIII with 1 pair of spinal setae, such as in Cerataphis and Tuberaphis (Fig. 3). In Nipponaphidini, typical embryonic setae pattern is head with 4 pairs of setae, each thoracic notum with 1 pair of spinal and 2 pairs of marginal setae, abdominal tergites I-VII each with 1 pair of spinal and 1 pair of marginal setae, and tergite VIII with 1 pair of spinal setae, such as in Dinipponaphis, Neothoracaphis and Sinonipponaphis (Fig. 4). Because of limited materials, just one genus of three genera in the world’ s known Hormaphidini was studied; thus there is not enough evidence in our results to judge its elementary setal pattern and development principles. The embryonic setal patterns of genus Doraphis in Cerataphidini and the genus Hamamelistes in Hormaphidini show the reduction of spinal and pleural setae on thoracic nota and the same placement of spinal setae on abdomental tergites IV-VIII. It seems that Doraphis is more similar to Hamamelistes in embryos than the genera in the same tribe. However, Doraphis also has horns on head vertex in 4th instar nymphs of alate viviparous females. This is a unique
character of Cerataphidini. Thus, the position of Doraphis is doubtful. Development of embryonic setal patterns Because the embryo is the first period of individual development, all embryonic characters are very important for phylogeny. Therefore, embryonic character variety can be used as an indication of the directions of systematical phylogeny in some respects (Richards, 1965). We provide a little more data on development of embryonic setal patterns among genera (Table 2). Compared with elementary setal patterns in Cerataphidini, the developement of embryonic setal patterns took two distinct directions (Fig. 3), one is with pleural setae on abdominal tergites unchanged in number and distribution, setae on pronotum increased and setae on head absent or displaced, as Pseudoregma, Astegopteryx, Aleurodaphis and Ceratovacuna on the one hand, and on the other is with pleural setae on abdominal tergites increased or absent, setae on thoracic nota decreased, and setae on head increased, absent or displaced, as with Chaitoregma, Doraphis, Ceratoglyphina and Glyphinaphis. In Astegopteryx, embryonic setal patterns become modified in two ways, one is with dorsal setae on head increased like A. bambusae (Fig. 1c), and the other is with pleural setae on abdominal tergite V absent like A. minuta (Fig. 1d). In Pseudoregma, embryonic setal patterns also have some differences in two ways: one is with pleural setae on abdominal tergite V absent and marginal setae on head displaced like P. bambucicola (Fig. 1m) and P. panicola (Fig. 1o), and the other is with 1 pair of setae on head and pleural setae on pronotum absent, and spinal setae on abdominal tergites VII－VIII displaced like P. alexanderi (Fig. 1l) and P. koshunensis (Fig. 1n). Compared with the elementary setal patterns in Nipponaphidini, the embryonic setal patterns took two distinct directions (Fig. 4): one is with spinal setae of abdominal tergites reduced in number, setae on thoracic nota added, reduced or displaced, and portion of distal setae on head modified, as Euthoracaphis, Quadrartus, Indonipponaphis, Metanipponaphis, Reticulaphis and Monzenia, and the other is with unchanged number of spinal setae on abdominal tergites, setae on thoracic nota increased or decreased, and distal setae on head increased or displaced, as Neonipponaphis and Quernaphis. Neoteny of setal patterns in adults Protopatterns of Hormaphidinae are typical embryonic setae patterns. But mesopatterns and metapatterns are
© 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
Genus
Neothoracaphis
Hormaphidini Hamamelistes 2 1, 0, 1
1, 1(forward), 1
2, 1, 1
1
Neonipponaphis 1
Quernaphis
1, 1, 1
1
Monzenia
1, 1, 1
1
Reticulaphis
0, 0, 2
1, 0, 2
2, 0, 2
1, 0, 2
2, 0, 2
1, 0, 2
1(forward), 1, 1 1, 0, 2(lateral)
1, 0, 2
1, 1(forward), 1
1, 1(forward), 1
1, 0, 2
1, 0, 2
1, 0, 2
Indonipponaphis 1
1
Quadrartus
1(forward), 1, 1
1, 1, 1
0, 1, 1
1, 0, 2
0, 0, 2
1, 0, 2
2, 0, 2
2, 1, 2
2, 1, 2
1, 0, 2
Pronotum
Metanipponaphis 1
1
Euthoracaphis
Sinonipponaphis
1
2
Glyphinaphis
1, 1, 2
1, 0, 1
2 2
2, 2, 0
2
1, 0, 0
1(pleural), 0, 1
2 2
1, 1(marginal), 1
1, 1, 1
2
2
Doraphis
NipponaphidiniDinipponaphis
Head Cephalic seta Dorsal seta
Ceratoglyphina
Chaitoregma
Ceratovacuna
Aleurodaphis
Astegopteryx
Pseudoregma
Tuberaphis
Cerataphidini Cerataphis
Tribe
Table 2 Embryonic setal patterns of genera in Hormaphidinae.
0, 0, 2
1, 0, 1
1, 0, 2
1, 0, 2
1(marginal), 0, 2
1, 0, 1
1, 0, 2
1, 0, 2
1, 0, 2
1, 0, 2
1, 1, 2
1, 1, 2
0, 0, 2
1, 1, 2
1, 1, 2
1, 1, 2
1, 1, 2
1, 1, 2
Mesonotum
Abd. Abd. Abd. Abd. Abd.
0, 0, 2
1, 0, 1
1, 0, 2
1, 0, 2
1, 0, 2
1, 0, 2
1, 0, 2
1, 0, 2
1, 0, 2
1, 0, 2
1, 1, 2
1, 1, 2
0, 0, 2
1, 1, 2
1, 1, 2
1, 1, 2
1, 1, 2
1, 1, 2
II III IV V VI VII
VIII
0, 0, 1 0, 0, 1 0, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 1, 0, 0
1, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 1, 0, 0
1, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 1, 0, 0
1, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 1, 0, 0
0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 1, 0, 0
1, 0, 1 1, 0, 1 0, 0, 1 0, 0, 1 0, 0, 1 1, 0, 1 0, 0, 1 1, 0, 0
1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 1, 1 1, 1, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 1, 1 1, 1, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 2, 1 1, 2, 1 1, 2, 1 1, 2, 1 1, 2, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 0, 1 1, 0, 1 1, 0, 0
1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 1, 1 1, 0, 1 1, 0, 1 1, 0, 0
I
tergite tergite tergite tergite tergite tergite tergite tergite
Abd.
notum
Abd.
Abd.
Meta-
346 L.Y. Jiang et al.
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Development of setal patterns on Hormaphidinae aphids 347
Fig. 3 Development of embryonic setal patterns in Cerataphidini.
© 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
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Fig. 4 Development of embryonic setal patterns in Nipponaphidini.
© 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
Development of setal patterns on Hormaphidinae aphids 349 Table 3 Setal patterns of adult viviparous females in Hormaphidinae. Tribe
Genus
Type
Head
Thoracic nota
Abdominal tergites
Cerataphidini
Cerataphis Tuberaphis Pseudoregma Astegopteryx Aleurodaphis Ceratovacuna
Apt. Apt. Apt. Apt. Apt. Apt. Ala. Apt. Ala. Apt. Apt. Ala.
MTP MSP MTP MSP MSP MTP MTP MTP MTP MTP PTP MSP
MTP MSP MTP MSP MSP MTP MTP MTP MTP MTP PTP MSP
Euthoracaphis
Apt. Ala. Apt. Ala. Apt.
PTP PTP PTP MSP MTP
PTP PTP PTP MSP MTP
Quadrartus Indonipponaphis Metanipponaphis Reticulaphis Monzenia
Ala. Ala. Apt. Apt. Apt. Ala.
PTP MTP PTP PTP MSP MSP
PTP MTP MSP MSP MSP MTP
Neonipponaphis
Apt.
MTP
MTP
Quernaphis Hamamelistes
Ala. Apt. Ala.
MSP MSP PTP
MSP MSP PTP
MTP MSP MTP MSP PTP MSP MSP MTP MTP MTP PTP MSP (tergites I-VII), MTP (tergite VIII) PTP MSP PTP MSP MTP (tergite I), MSP (tergites II-VIII) PTP MTP PTP PTP MTP MSP (tergites I-VII), MTP (tergites VIII) PTP (tergites I, V-VII), MTP (tergites II-IV, VIII) PTP MSP PTP
Nipponaphidini
Chaitoregma Doraphis Ceratoglyphina Glyphinaphis Dinipponaphis Neothoracaphis Sinonipponaphis
Hormaphidini
PTP = protopattern; MSP = mesopattern; MTP = metapattern. Apt. = apterous viviparous females; Ala. = alate viviparous females.
various in tribes (Table 3). Some mesopatterns or metapatterns are typical. However, some of them have mixed characters of protopatterns or of protopatterns and mesopatterns. In Cerataphidini, mesopatterns differ from protopatterns mainly by having more hairs of pronotum, and hairs of head, mesonotum, metanotum and abdominal tergites partly remain the same as protopatterns until adulthood. Metapatterns are typical or composed of protopatterns and mesopatterns. In Nipponaphidini, mesopatterns mainly have dorsal hairs increased on head, thoracic nota and abdominal tergites, respectively. But metapatterns have almost been replaced by mesopatterns in adults. Thus, neoteny based on the research of setal patterns is not as remarkable as that in each group of
Hormaphidinae. Most neoteny is complex with various setal patterns on each part of body, especially in Nipponaphidini. Neoteny on abdominal tergites is most distinct and has the highest diversity, since it appears frequently with protopatterns or mesopatterns on abdomens and sometimes has different patterns in each tergite. Head and thoracic nota often express neoteny together and almost have the same form as protopatterns or mesopatterns. Different type of adult viviparous females also shows different neoteny, even in the same species. The common results of Hamamelistes in Hormaphidini and Drepanosiphidae (Qiao & Zhang, 2003) indicate that apterous viviparous females usually have much more hair and less neoteny than alate viviparous females. However, in
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adult of Nipponaphidini, apterous viviparous females show more neoteny than alate viviparous females. Because apterous viviparous females in the tribe are very special with segments sclerotized and fused distinctly, generally have the same setal patterns as embryos, and then have fewer dorsal hairs than alate viviparous females, except for Euthoracaphis. But there are no obviously differences in Cerataphidini. Based on our observations, we consider setal patterns of the abdominal tergites as the most important characters in embryonic and adult setal patterns, and that neoteny is an established pattern in some Hormaphidinae. The genera with neoteny are more advanced than those without neoteny, even those with partial neoteny. This conclusion agrees with that in Drepanosiphidae (Richards, 1965, Qiao & Zhang, 2003). In the Hormaphidinae, Nipponaphidini and Hormaphidini have more typical neoteny than Cerataphidini.
Acknowledgments The authors are wish to thank Dr. M. Sorin (Sakuragaoka, Ise, Mie, Japan) for his loan of specimens, to Mr. Tie-Sen Zhong for collecting samples, to Ms. Cai-Ping Liu for making slides and to Mr. Pei-Ming Wang for his help with some of the figures. The project was supported by the National Natural Sciences Foundation of China (Grant No. 30570214, No. 30670240), and National Science Fund for Fostering Talents in Basic Research (Special subjects in animal taxonomy, NSFC-J0630964/J0109).
References Börner, C. (1930) Beiträge zu einem neuen System der Blattläuse. (l. Mitteilung.). Arch. Klassifikator. Phylogenet Entomology, 1, 115-194. Noordam, D. (1991) Hormaphidinae from Java (Homoptera, Aphididae). Zoologische Verhandelingen, 270, 1-525. Qiao, G.X. and Zhang, G.X. (2001) A study on the genus Cerataphis Lichtenstein from China with the description of one new species (Homoptera, Hormaphididae). Acta Entomologica Sinica, 44, 555-559. Qiao, G.X. and Zhang, G.X. (2003) Development of setal patterns in embryonic and adult Drepanosiphid aphids (Homoptera, Aphidoidea, Drepanosiphidae). Acta Zootaxonomica Sinica, 28, 573-583. (in Chinese with English summary) Remaudière, G. and Remaudière, M. (1997) Catalogue of the World ’s Aphididae. Institut National de la Recherche Agronomique, Paris, 473 pp. Richards, W.R. (1965) The Callaphidini of Canada (Homoptera: Aphididae). Memoirs of the Entomological Society of Canada, 44, 1-149. Webster, F.W. and Phillip, W.J. (1912) The spring grain-aphids or“ green bug”. U. S. Department of Agriculture Bureau. Entomological Bullitin, 110, 1-153. Zhang, G.X., Zhang, W.Y. and Zhong, T.S. (1991) Studies on the genus Tetraneura Hartig, 1841 from China (Homoptera, Pemphigidae) with descriptions of new species and subspecies. Sinozoologia, 8, 205-236.
Accepted April 2, 2007
© 2007 The Authors Insect Science (2007) 14, 339-350 Journal compilation © Institute of Zoology, Chinese Academy of Sciences
