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Corresponding author: Zhengyang Liu ( saturniidae@qq.com ) Academic editor: Andreas Zwick
© 2024 Zhengyang Liu.
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The moth genus Sinobirma was reared successfully for the first time, based on specimens of Sinobirma bouyeri collected in the southeastern Himalayas of Tibet. Larvae were reared on the host plants Coriaria nepalensis and Prunus cerasoides in captivity in Yunnan. Morphology and biology of the ovum, larvae, and pupa of S. bouyeri are described in detail. The species exhibits strong gregarious behavior during all larval instars, with mature larvae of S. bouyeri primarily feeding at night. The larvae are black and decorated with green stripes, pupating individually in the soil. Numerous host plants known to be used by African and Asian Saturniidae were tested with larvae of this species. The first parasitoid for the genus Sinobirma is reported. The complete mitochondrial genome was sequenced and used to reconstruct a molecular phylogeny to test the tribal placement of Sinobirma. The paper provided further evidence that Sinobirma originated from the African mainland and reached the Himalayas through dispersal.
Africa, biogeography, China, chaetotaxy, ecology, fluorescence, Himalayas, India, mitochondrial genome, life-history, morphology, Myanmar, parasitoid, phylogeny, SEM, Urotini
Despite being one of the most enigmatic members of the Asian fauna of Saturniidae, the complete life history of the genus Sinobirma Bryk, 1944 has remained unknown. Currently, only four taxa are included in the genus, which is now regarded as a member of Urotini, all other genera of the tribe are distributed in mainland Africa and Madagascar in contrast to the Asian Sinobirma (Rougerie et al. preprint). Due to the restricted and isolated occurrence of Sinobirma in the eastern end of the Himalayas, only a few reports and studies on the genus have been published in the past. Consequently, the biology and evolutionary history of Sinobirma have remained one of the largest mysteries in the study of Saturniidae so far.
Swedish entomologist René Malaise tested his famous design of an insect trap (the Malaise trap) during an expedition to northeastern Burma in 1934, specifically around Kambaiti [Kanpaikti Sub-Township (the local official spelling today)], in Kachin State of Burma, only about 1 km from the border of the Chinese province Yunnan. Using these traps and light, René and his wife Ebba Malaise collected a large number of lepidopterous specimens (
After half a century of silence, Bryk’s taxonomic opinion was challenged.
About 70 years after Malaise’s entomological excursion, seven males and four females of S. malaisei were collected by Rodolphe Rougerie in Tongbinguan [sic] [Tongbiguan, Yunnan], a nature reserve near the type-locality at an elevation of 2080 m, during the nights of 12–13 June 2001.
The record of one additional male of S. malaisei was reported by
The genus Sinobirma had long been overlooked in China. Other than
Based on live material from Yunnan,
More recently,
All aforementioned records of Sinobirma are from mid-altitude regions (ca. 1000–2500 m) in humid subtropical northern Burma, southwestern China and northeastern India, mainly for May–June. Therefore, all three species are likely univoltine summer flyers in the southeastern Himalayas. Apart from Burma, the genus has not been reported from any other areas of the Indochinese Peninsula.
To learn more about the biology and evolutionary history of the genus Sinobirma, this study explores and documents the complete life-cycle of a representative species, S. bouyeri, for the first time. This includes tests of dozens of putative host plants, and the discovery of the first parasitoid. Furthermore, this study aims to test evolutionary and biogeographic hypotheses proposed in earlier literature (
General equipment and usage: Vernier caliper INSIZE 1108-150C 0–150 mm / 0.01 mm (± 0.02 mm) and measuring microscope PEAK 2008-50X 0–1.6 mm / 0.02 mm were used to measure general lengths of immature material and to calibrated scale bars shown in figures. Balance XINGYUN FA1204E 120 g / 0.0001 g (± 0.0002 g) was used to determine the mass of pupae. Illuminometer BENETECH GM1020 (≤ 10000 Lux ± 3%; ≥ 10000 Lux ± 4%) was used for recording illuminance in the study of larval circadian rhythm. Fluorescent tubes PHILIPS TL 6W (UV-A, peak: 365 nm), QIANPU UVB-313EL 6W (UV-B, peak: 313 nm) and PHILIPS TUV 6W (UV-C, peak: 254 nm) were used for fluorescence tests and photographs of mature larvae. Soil pH, humidity and temperature were recorded by a data logger SMART SENSOR PH328 (± 0.2 pH; ± 4 RH%; ± 1.5°C), while hygrothermograph BENETECH GM1365 (± 2 RH%; ± 0.3°C) was used for recording of relative humidity and temperature during rearing. All color figures were photographed with a NIKON D5500 DSLR with SIGMA 10–20 mm f/4–5.6 lens or LAOWA 60 mm f/2.8–22 lens. Scanning electron microscope [SEM] images were taken with a ZEISS GeminiSEM 360. SEM samples of S. bouyeri were surface-dried and sputter-coated: Two unhatched ova, two larval head capsules of each L1 and L5, and one whole L1 larva. Scoli and their distribution map in Fig.
In 2020, I received papered females of S. bouyeri from southeastern Tibet. One ♀ had been collected at the type-locality Bomê County, 2111 m, on 23 June, and 2 ♀♀ had been collected in Nyingchi City, 2052 m, on 22 June. From all of these, only one egg was obtained, off-white in color and not hatching during that year. I opened it on 05 April 2021; there was no embryo inside. During my expedition to the southern border of Tibet in the summer of 2021, 2 ♂♂ and 1 ♀ of S. bouyeri were captured during the nights of 26–29 June, at 2134 m in Mêdog County. Unfortunately, this female also laid only a single ovum in the paper triangle envelope, and it was lost on the following ecological survey. On 17 June 2022, I went back to the place, 12 ♀♀ and 3 ♂♂ were collected during the next 10 days. The females finally oviposited in a closed cylindrical net-cage (1.8–2.2 mm mesh), which was hung outdoors away from the vegetation in Mêdog. These caged eggs were later collected into a gauze bag (single mesh opening width: ca. 0.1 mm) and driven back to the research site in Kunming City, Yunnan, at an elevation of 1940 m. The eggs were placed indoors in a gauze cage (0.3 mm mesh) on a piece of mesh suspended ca. 1 cm above a moisture-saturated cotton pad, and sprayed with water every day. The resulting air humidity surrounding the eggs was ca. 80–95% RH at a temperature of ca. 17–21°C.
Newly hatched caterpillars were offered a large variety of host plants. A total of 35 species within 26 families of plants were chosen for the tests to larvae (sections 3.2.1–3.2.26), including 11 families commonly fed by African saturniids, and several families used to breed Asian species in the subfamilies Saturniinae, Salassinae and Agliinae. Also plants from a few other families found in the natural habitat of S. bouyeri were offered. All plants were collected in northern Kunming at elevations of ca. 1800–2000 m, using only fresh stems and leaves without pesticide contamination. Newly hatched larvae were offered plants the same day and sealed with just one plant species each in a plastic zip lock bag for observation. Feeding behaviour was recorded after 24 hours, and larvae that rejected their plant were switched to another plant species for testing. If feeding was confirmed, the lower parts of the plant’s stems were inserted into a bottle filled with water (gaps in the bottleneck were closed with tissue paper). Plants with larvae were placed in a separate cage to continue observations indoors or outdoors.
After feeding had ended (after the liquid defecation), larvae were placed in a container with 9–10 cm of loose and uniform peat soil at the bottom for pupation (peat had been produced naturally from Heilongjiang Province of China; ca. 0.35–0.47 g/cm³ with moisture and holes, pH 6.28–6.51, 20.8–24.3°C and 52.6–61.4% RH). The soil surface was covered with ca. 1–2 cm of Sphagnum moss (Sphagnaceae) and several fallen walnut leaves.
This work supplements here a circular sequence of the complete mitochondrial genome of S. bouyeri [GenBank: OR754233], its specimen data and high-throughput files have been uploaded to NCBI [BioProject: PRJNA905660].
DNA sequence data were generated from a fresh L4 caterpillar of S. bouyeri [BioSample: SAMN31802199], which was killed and preserved in 95% (± 5%) ethanol at –18°C. DNA was extracted with chloroform-isoamyl alcohol and fragmented by ultrasonication. DNA library preparation (Illumina DNA Prep #1000000025416) included end repairing, 3’-end adenylation and ligation of sequencing adapter. Size selection was carried out on an agarose gel prior to amplification by PCR. After clean up and check, qualified libraries were sequenced on an ILLUMINA NovaSeq 6000. The resulting data [SRA: SRR22414765] were de novo assembled with SPAdes 3.15.4 (
Linear map of the complete mitochondrial genome of Sinobirma bouyeri [OR754233].
Phylogenetic trees (Fig.
T1–A10 Chaetotaxy [primary setae] of Sinobirma bouyeri L1 in lateral view, not shown the setae of head capsule and legs T1–3, and proleg A10 displays the medial surface, the ventral midline constitutes the bottom margins of A1–9; B guidelines, the gray rectangle represents “lateral”; C, E–H Warts of Sinobirma bouyeri L5; C chalaza (e.g., V-I, SV-I, D-I); E bifurcated scolus with a small (e.g., L-II, D-II) or medium-sized base (e.g., XD-II); F asterisk-like scolus with a small base (e.g., SV-III); G asterisk-like scolus with a medium-sized base (e.g., L-III, SD-III); H asterisk-like scolus with a large base (e.g., D-III).
MAFFT V7 (
Homology of morphological structures, chaetotaxal terminology and its abbreviations follow
The information provided in this section is based specifically on the S. bouyeri as a representative of the genus Sinobirma.
In the sections 3.1.1–3.1.7, the lengths, widths, heights, and quantitative statistics (e.g., the quantity of setae and crochets) are based on single individual observations, unless otherwise specified. The widths of head capsules (for each sample, it is the distance between the pair of S6) are derived from the optimal host plant from the tests (see section 4.2).
Elongated sphere (length 1.71 mm, width 1.16–1.21 mm; n = 8); the micropylar area is located on the slightly more flattened short end (Fig.
Ova of Sinobirma bouyeri. A Lateral view, scale bar = 400 µm; a: micropylar side; b: non-micropylar side. B Non-micropylar side, vertical view, scale bar = 350 µm. C Micropylar side, vertical view, scale bar = 350 µm; a: micropylar zone. D A part of exochorion in the non-micropylar area, scale bar = 40 µm. E Aeropyle, scale bar = 4 µm. F Aeropyle, scale bar = 3 µm. G Micropylar zone, scale bar = 20 µm; a: central area; b: foreign matter.
Head capsule. Cervacoria is translucent dark gray; the width of the shiny black head capsule is 837.2 μm, with a dark grey anteclypeus; the 17 longer primary setae are borne on the head capsule, i.e., P1, P2, L1, AF1, AF2, F1, C1, C2, A1, A2, A3, O1, O2, O3, SO1, SO2 and SO3 (Fig.
L1 of Sinobirma bouyeri. A–E Cephalic regions. A Frontal view, scale bar = 200 µm. B Lateral view, scale bar = 100 µm; a: head capsule; b: antenna; c: mandible; d: maxilla-hypopharynx-labial complex. C Frontal view, scale bar = 100 µm; a: head capsule; b: anteclypeus (a part of the head capsule); c1–3: the 1st–3rd antennal segments; d: labrum; e: mandible; f: maxilla; g: hypopharynx. D Frontal view, scale bar = 100 µm; a: frons; b: clypeus; a + b: frontoclypeus; c: anteclypeus; d: other area of the head capsule. E Posterior view, scale bar = 200 µm. F Leg T3, apical view, scale bar = 40 µm; a: coxa; b: femur; c: tibia; d: tarsus; e: pretarsus. G Prothoracic shield, frontal view, scale bar = 100 µm. H Prothoracic shield, ventral view [the inner surface], scale bar = 100 µm; a: secondary seta.
L1 of Sinobirma bouyeri. A–M Cephalic regions. A Head capsule, frontal view, scale bar = 50 µm. B Head capsule, frontal view, scale bar = 20 µm. C Head capsule, frontal view, scale bar = 50 µm. D Posterior view, scale bar = 80 µm; a: head capsule; b: labrum; c: mandibles; d–j: maxillae; d: cardines; e: stipites; f: palpifers; g–i: the 1st–3rd maxillary palpal segments; j: maxillary mesal lobes; k–q: labium; k: submentales l: postmentum; m: mentum; n: prementum (posterior); o: spinneret; p: labial palpi; q: prementum (anterior). E Lateroapical view, scale bar = 30 µm; a: antacoria; b–d: the 1st–3rd antennal segments. F Dorsal view, scale bar = 40 µm; a–c: the 1st–3rd maxillary palpal segments; d: maxillary mesal lobe. G The 2nd–3rd maxillary palpal segments, dorsoapical view, scale bar = 10 µm. H The distal area of maxillary mesal lobe, dorsal view, scale bar = 20 µm. I The distal area of labial palpus, ventral view, scale bar = 10 µm. J Seta P1, scale bar = 50 µm. K Seta MD2, scale bar = 5 µm. L Seta MD1, scale bar = 4 µm. M Part of the external surface [epicuticle] of S3, scale bar = 4 µm.
Antenna. The 2nd segment of the antenna has the largest exposed areas (Figs
Mouthparts. Primary setae L1, L2, L3, M1, M2 and M3 (Figs
Thorax and abdomen. The chaetotaxy is as illustrated (Fig.
Sinobirma bouyeri L1, a quantity statistic of chalazae/scoli (outside brackets) on the single side (divided along the dorsal and ventral midlines), with the numbers of primary setae (inside brackets) borne on each of them. See also Fig.
Structures\Segments | T1 | T2–3 | A1 | A2 | A3–6 | A7 | A8 | A9 | A10 |
Scoli D-III | 1(5) | 1(4) | 1(4) | 1(4) | 1(4) | 1(3) | 1(4) | ||
Scolus D-II | 1(2) | ||||||||
Chalazae D-I | 2(1) | 1(1) | 1(1) | 1(1) | 1(1) | 1(1) | 1(1) | ||
Scolus XD-II | 1(2) | ||||||||
Scoli SD-III | 1(4) | 1(4) | 1(4) | 1(4) | 1(4) | 1(4) | 1(4) | 1(3) | |
Scoli L-III | 1(6–7) | 1(5) | 1(6) | 1(6–7) | 1(6) | 1(6) | 1(6) | ||
Scoli L-II | 1(2) | 1(2) | 1(2) | 1(2) | 1(2) | 1(2) | |||
Scoli SV-III | 1(4) | 1(3) | |||||||
Chalazae SV-I | 1(1) | 1(1) | 2(1) | 1–2(1) | 1(1) | 1(1) | |||
Chalazae V-I | 3(1) | 3(1) | 1(1) | 1(1) | 1(1) | 1(1) | 4(1) |
The width of head capsule increases to 1.31 mm. Many secondary setae are visible on the integument, especially the ventral area. In dorsal view, T1–A10 are black in color, with discontinuous pale yellow middorsal stripes on T1–A8. The bases of scoli D-III are still prominent and are the largest; scoli D-III, XD-II and SD-III have shiny red bases and bear reddish orange spiny setae, with the setae of scoli XD-II and SD-III of T1 the longest. Chalazae SV-I, scoli L-II and L-III have ochre bases, while scoli SV-III and chalazae V-I have gray bases. The ventral area of T1–3 is dark gray, but it is yellowish for A1–10. For each of the legs T1–3, the pretarsus and tarsus are dark maroon, the tibia and femur shiny black, and the coxa gray. The posterolateral margins of prolegs A10 are ocher around their lateral plates. Pale yellow stripes, discontinuous and nearly crescent-shaped, are visible between the scoli D-III and SD-III on A1–8, and likewise some irregularly shaped stripes of the same color around the black spiracles of these segments. In lateral view, the dorsal junction area between A1/A2 is the most sunken area, conspicuous when a larva rests on a plant. Prolegs, plantae and crochets of A3–6 and A10 are identical in color as in L1, but the plantae are wider and bear uniserial homoideous mesoseries of 24–26 crochets.
Head capsule is 2.17 mm in width. The prothoracic shield starts to split along the dorsal midline, in some individuals this “fissure” appeared as multiple irregular and discontinuous depressions. The ventral areas of most segments are gray, but fade to yellow on A7–9. A larger number of minute, white secondary setae are visible in the dorsal area, especially around D-III — a scolus significantly more elevated than in the L2 and with its inferior basal parts turning into a smooth black, but the superior area shiny red. Each scolus D-III bears strong brown spines, but the longest setae are still those on scoli XD-II and SD-III of T1. Except for those in the middorsal area, the yellow stripes described in L2 are vivid lime green, especially in the lateral areas of T1 and A1–8. All proleg bases and plantae look more developed and inflated than in L2. All prolegs have a goldenrod ground color, and each of them exhibits 42–45 reddish brown crochets in biordinal mesoseries. The posterior tip of the shiny black anal shield is more elongate than in L2.
Head capsule width is 3.24 mm; the shiny black prothoracic shield has a fissure along the dorsal midline, but it isn’t fully split yet. All the bases of scoli are shiny black, most of them with translucent brown spiny setae, but the strongest and longest setae of scoli D-III have turned into almost opaque black. The bases of scoli XD-II and SD-III on T1 are significantly more elevated than in L3. Ground color of the whole ventral area is brownish gray, and T1–A10 bear more white secondary setae on the lateral areas of the integument. There are several lime green “Y-shaped” strips ornamenting the dorsal midline of T2–A8. The lateral stripes that appeared in L2 are wider and developed into lime green patches, the largest ones of which have black dots in their centers on A1–8. On each side of A1–7, an ochre strip connects scolus D-III, scolus SD-III and the spiracle. The lateral plates of prolegs A3–6 and A10 are black and smooth; their plantae are vivid yellow, each bearing 50–55 maroon crochets arranged in biordinal mesoseries. The posterior margin of the anal shield is elongated into a short spine, more pronounced than in L3.
This is the final larval instar under normal conditions (but see section 3.2.10 for a case of L6). The head capsule is 4.74 mm in width. Its epicranial suture, ecdysial lines, anteclypeus and the antacoriae are off-white. The medial margin of the labrum is bronze color, the frontoclypeus a dark brown with a pair of triangular black spots in its center (Fig.
L5 of Sinobirma bouyeri. A Head capsule, frontal view, scale bar = 800 µm. B Head capsule, frontal view, scale bar = 500 µm. C Frontal view, scale bar = 300 µm; a: labrum; b: mandibles. D Posterolateral view, scale bar = 500 µm; a: head capsule; b: antacoria; c1–3: the 1st–3rd antennal segments; d: mandible; e: maxilla-hypopharynx-labial complex. E Posterior view, scale bar = 200 µm; a: head capsule; b: antenna; c: mandibles; d–j: maxillae; d: cardo; e: stipites; f: palpifers; g–i: the 1st–3rd maxillary palpal segments; j: maxillary mesal lobes; k–m: labium; k: postmentum; l: mentum; m: prementum (posterior). F Lateroapical view, scale bar = 200 µm; a–c: the 1st–3rd antennal segments. G Ventroapical view, scale bar = 80 µm; a–b: the 2nd–3rd maxillary palpal segments. H Maxillary mesal lobe, ventral view, scale bar = 60 µm. I labial palpus, medioapical view, scale bar = 40 µm. J ♂, ventral view, scale bar = 1 mm; a–c: A8–10. K ♀, ventral view, scale bar = 1 mm; a–c: A8–10; d: sexual gland. L Ventral view, scale bar = 2 mm; a1–3: coxal sclerites T1–3.
Larvae of Sinobirma bouyeri. A, G–O Reared on Coriaria nepalensis; B, D–F Reared on Prunus cerasoides; C Reared on Salix babylonica. A L1, lateral view, scale bar = 1 mm. B L1, dorsal view, scale bar = 1 mm. C L2, lateral view, scale bar = 2 mm. D L2, dorsal view, scale bar = 2 mm. E L3, lateral view, scale bar = 3 mm. F L3, dorsal view, scale bar = 3 mm. G L4, lateral view, scale bar = 5 mm. H L4, dorsal view, scale bar = 5 mm. I Freshly moulted L5, lateral view, scale bar = 5 mm. J L5, lateral view, scale bar = 7 mm. K L5, dorsal view, scale bar = 7 mm. L L5, ventral view, scale bar = 7 mm. M Planta A4 of L5, ventrolateral view, scale bar = 1 mm. N A8–10 of L5, lateral view, scale bar = 3 mm. O Cephalic regions and T1–2 of L5, anterolateral view, scale bar = 2 mm.
Compared to L4, the general habitus of L5 is nearly identical, with a cylindrically shaped larva that has the largest volume in A3 and A4. The most obvious difference to L4 is that the lime green middorsal strips are wider, and that similar strips are now visible in the dorsal area of A9–10. Many white secondary setae cover the larval integument; they are more numerous and visible than in previous instars, especially on the lateral and dorsal areas. The fusion of scoli D-III of A8 is identical as in L1.
In freshly molted specimens, most parts of the legs T1–3 (except the dark maroon pretarsi), most parts of the prolegs A3–6 (except the reddish maroon crochets), all chalazae/scoli, the head capsule and the whole A10 are bright goldenrod; these structures darken in fully hardened and tanned larvae (Fig.
As in L2–4, the dorsal area of the A1/A2 junction zone (sometimes together with T3/A1) can be observed as the most sunken area in lateral view. The shiny black prothoracic shield splits into two parts along the off-white middorsal fissure in L5. The anal shield is large and triangular, its posterior tip distinctly elongated to form a strong spine as in L4 (Fig.
The overall color of the epicuticle is black, but A4–8 appear dark reddish brown. Female pupae are generally larger. The antennal margins are slightly elevated in males (Fig.
Pupae of Sinobirma bouyeri. A Scale bar = 10 mm; a: ♂, lateral view; b: ♂, ventral view; c: ♂, dorsal view; d: ♀, lateral view; e: ♀, ventral view; f: ♀, dorsal view. B ♂, ventral view, scale bar = 1 mm; a–b: A8–9; c: genital pore. C ♂, ventrolateral view, scale bar = 2 mm; a: antenna; b: head tubercles. D ♀, ventral view, scale bar = 1 mm; a–b: A8–9; c–d: genital pores. E ♀, ventrolateral view, scale bar = 2 mm; a: antenna; b: head tubercles. F ♀, lateral view, scale bar = 1 mm; a–b: A4–5; c: abdominal tubercles; d: annular cap of spiracle. G ♀, anterolateral view, scale bar = 2 mm; a–c: T1–3; d: thoracic tubercles; e: annular cap of spiracle T1. H ♀, the long spiny cremaster on the tip of A10, scale bar = 2 mm; a: ventral view; b: lateral view; c: dorsal view.
Host plant preference was systematically tested by restricting batches of larvae to just one plant at a time, and observations are presented by plant family in the following sub-sections. To reduce the risk of larval infectious diseases for larvae indoors, the rearing density had to be reduced. Therefore, some of the larvae from plants discussed in sub-sections 3.2.4, 3.2.5, 3.2.10, 3.2.14, 3.2.22 and 3.2.24 were placed onto wild trees. This also provided an opportunity to collect potential parasitoids in the wild of Yunnan. However, all of these caterpillars were missing within a week, most probably preyed upon or having left the plants by themselves.
The larval group rejected Sapindus saponaria, but easily accepted Acer buergerianum after switching. Unfortunately, all of the ten individuals died together on the 4th day after feeding.
None of the larvae (ten larvae each) accepted Puhuaea cf. sequax or Albizia julibrissin, but ten other larvae formed a cluster and quickly accepted Robinia pseudoacacia. These feeding larvae started to die after the 4th day, became restless (left the host plant) and finally all died before the first pre-molt, achieving a lifespan of only 4–8 days.
Pistacia weinmanniifolia was quickly accepted by ten larvae, and these larvae increased visibly in size by the 3rd day. However, the following day most of the individuals moved restlessly and died the next day. The last larva died on the 7th day. A different batch of ten larvae performed similarly on Pistacia chinensis. Two batches of ten larvae each fed on Rhus typhina and Toxicodendron vernicifluum, but began to die from the 3rd day. No larvae survived to L2 on host plants of this family.
The early development of 19 larvae on Salix babylonica was rapid during the first three days, but progress in growth started to vary significantly between individuals from the 6th day of L1, because some individuals frequently left the larval cluster, causing inconsistency in their feeding behavior. All individuals molted from L3 to L4 on days 26th–31st, despite their variations in size; two larvae died of illness during L3. The remaining 17 L4 of this group died, either by sampling four specimens for morphological studies or when releasing them on a willow tree outdoors for further observations.
Two groups of 10 larvae each were offered Quercus yunnanensis and Quercus glaucoides. As the leaves of the former were too hard, all individuals were switched to Q. yunnanensis on the 3rd day. These 20 larvae, which had all hatched on the same date, soon formed a single cluster and continued to feed. However, larval growth began to slow significantly from the 4th day, and a total of 6 individuals had died by the 7th day, while other larvae often crawled around restlessly. Consequently, oaks were judged to be unacceptable host plants in captivity. On the 7th day, before the first pre-molt, all of the remaining 14 individuals were taken to the same plant outdoors for continued observation.
A group of 12 larvae was offered Toona sinensis. A minute gap in the edge of a leaf was observed on the 2nd day, but no further feeding occurred, and these larvae starved to death on the 4th day.
The genus Rhododendron forms one of the most spectacular plant communities in the alpine ecosystem of the Himalayas. I encountered them in abundance as shrubs during my expeditions to Mêdog, at altitudes from about 1500 to 4100 m, distributed from humid subtropical forests to snow lines. However, Rhododendron cf. pulchrum was rejected by all ten larvae in my test.
Similar to larvae on other host plants tested, a group of ten larvae quickly formed a tight cluster on a leaf of Hibiscus syriacus, but showed no sign of feeding on this plant.
Only the evergreen plant Cinnamomum camphora was tested for this family, but rejected by all ten larvae.
One of the first plants to be tested was Prunus cerasoides. Seventeen newly eclosed larvae easily accepted the plant, and an increase in size was observed for each specimen on the 3rd day. Larvae began to show differences in size starting with L3, and burrowed in the soil as L5. However, two larvae failed to pupate in the soil, while a single specimen molted to a weak L6. The rearing of these larvae was documented in more detail (Table S1).
A further ten larvae were tested on Pyrus pseudopashia with similar result after three days, but since P. pseudopashia was scarce near the experimental site, the larvae were switched to P. cerasoides on the 4th day, which larvae quickly accepted and continued to grow. An additional 70 larvae that had rejected other plants were added, resulting in a total of 80 larvae of different ages feeding on P. cerasoides. As rearing progressed, only one larval molting failed from L3 to L4, and a further six specimens died of illness during L2–4. The remaining larvae were released outdoors on P. cerasoides for further observation before entering L5.
A group of 8 larvae were tested on Rosa cf. multiflora, but they began to die from the 5th day onwards (L1). The last larva died as an early L2, resulting in lifespans of only 5–12 days.
During the field surveys in Mêdog and Bomê, Magnolia spp. were commonly encountered in the natural habitats of S. bouyeri. Therefore, Magnolia denudata was offered to ten larvae, but fully rejected.
Alnus nepalensis appears to form dominant populations in the Sub-Himalayan valleys where I collected the adults of S. bouyeri, but the ten larvae offered this plant rejected it without any bite marks on the leaves.
Liquidambar formosana is one of the most commonly used host plants when rearing many Asian saturniids in captivity. A batch of ten larvae started to feed on this plant, while another seven larvae rejected it and clustered on the inner wall of the zip lock bag. Larvae that fed on the plant did not increase significantly in size during the first three days and died one by one before the first pre-molt, resulting in lifespans of 3–7 days.
A total of ten larvae fed on Lagerstroemia indica, readily accepting the plant and growing faster than most others during the first 3 days. Therefore, an additional ten larvae that had rejected another plant were added. The hatching dates of the two larval batches differed by one day, but they soon formed a unified larval cluster. However, because some larvae aggregated at the mouth of the bottle, their feeding duration began to differ. The larvae eventually completed their first molt on the 8th–9th day after their respective hatching. Since L2, growth rate of larvae slowed significantly, with size differences between individuals increasing. By the 19th day, all larvae were still in L2 without pre-molt, making it the slowest batch to grow. Except for four larvae killed for morphological studies, the remaining 16 larvae were released on L. indica outdoors for continued observation.
Osyris lanceolata is a common shrub in southeastern China, but all ten larvae rejected the plant.
Plants of this family are very useful for rearing a large number of saturniid species from around the world. Walnut tree is common in southern Tibet and western Yunnan. A batch of seven larvae fed on Juglans regia from hatching to first molting for 13 days, which is the longest of all comparable batches on other plants. Two larvae died on the 3rd day after entering L2, and others died the following day.
A batch of ten larvae quickly accepted Ulmus parvifolia on the day of hatching, but all larvae died on the 4th day.
Coniferous forests are very common in the southern Himalayas, usually huge trees with a height of tens of meters. When tested with ten larvae, Keteleeria evelyniana was rejected outright.
Plants in the genus Zanthoxylum were found in the habitat of S. bouyeri in Mêdog, therefore, Zanthoxylum armatum was tested as a host for ten larvae. Only minimal bite marks were observed after two days, and 4 larvae had starved to death on the 3rd day. The plant was finally considered to be rejected, and the remaining larvae were transferred to other plants for testing.
The family Vitaceae was observed throughout the Tibetan habitats of S. bouyeri, but the vine Parthenocissus semicordata was rejected by all ten larvae.
A representative of Nyssaceae, Nyssa sinensis, was accepted by ten larvae, but all of them died in L1 on the 7th–9th day.
A few plants of Symplocos paniculata were found to grow naturally in the same region as S. bouyeri. Ten larvae readily accepted the plant within a day and produced feces. However, since only a seedling of the plant was near the experimental site, the indoor experiment had to be terminated on the 3rd day.
The evergreen shrub Camellia sasanqua was accepted by ten larvae on the 2nd day after hatching. However, the gnawing marks on the edges of the leaves weren’t obvious, and larvae actively left the host plant on the 3rd day and did not return to the plant on the 4th–5th days. Eventually, they starved to death in the cage.
Initially, only ten larvae were tested with Coriaria nepalensis (Fig.
Larvae of the second, larger group had had a later hatching date than the ten larvae in the first group, but all individuals in L2 entered the pre-molting state on the same day (21 Jul. 2022). During L4, the ten larvae from the first and 23 larvae from the second group were released outdoors on 04 Aug. 2022. One of the remaining 20 larvae was killed for morphological studies during L5, while the remaining 19 larvae completed their larval instars successfully and pupated in the soil. Apart from slight differences in the size of mature larvae, possibly due to gender, larvae across all groups reared on C. nepalensis maintained perfect developmental consistency during their L1–4, with none of the larvae leaving the host plant restlessly before feeding ended. The mature larvae were very strong and fully expressed some of their biological habits. Details of their complete larval development are given in Table S1.
Ten larvae were tested with Bischofia polycarpa, which they fed on quickly. However, the larvae didn’t grow and finally died within a week.
This plant family is widely used to rear larvae of many saturniids in captivity from around the world. Six larvae were presented with Ligustrum lucidum, but all individuals died during the 3rd–4th day after feeding.
Mêdog is located on the southern side of the Himalayas, and was the main area where S. bouyeri was collected. At this locality, these moths were observed under lamps at altitudes of 1953–2150 m in valleys (Fig.
During surveys at 1300–2400 m, local Lhoba people confirmed that there was snow cover every year in December and January. A total of 6,707 outdoor climatic data points was collected in Mêdog at 2134 m during 19–26 June 2022 (Table S2). Temperatures ranged from 14.3 to 27°C (average: 18.4°C), while relative humidity ranged from 54.2 to 98.7% (average: 89.4% RH).
All data of times mentioned in the sections 3.4.1–3.4.4 are based on UTC+8.
Unfortunately, the precise time of flight of each individual wasn’t recorded during light collecting, but the adults arrived at the light within three hours after full sunset (locally ca. 21:00). The moths are inactive during the day unless disturbed, and their eye spots on the hindwings are usually covered by the forewings while at rest (Fig.
Sinobirma bouyeri. A–E Adults; F–G ova. A ♀, resting position, dorsal view, scale bar = 20 mm. B ♀, startled, dorsal view, scale bar = 20 mm. C ♂, resting position, dorsal view, scale bar = 20 mm. D Pre-oviposition, scale bar = 20 mm. E Oviposition, scale bar = 5 mm. F Oviposition, scale bar = 3 mm. G Ova, scale bar = 2 mm.
Because the abdominal tip of female moth couldn’t move freely while passing through the cage mesh, the ova attached on the external surfaces of the cage usually formed irregular clusters. However, the ova collected from the inner surfaces of the cage were arranged side by side into parallel and single–tiered rows, in some cases overlapping into orderly clusters of 2–6 tiers. A total of 419 eggs was oviposited during 21–29 Jun. 2022. Only 53 ova remained unhatched by 25 Jul. 2022, ten of which were randomly dissected, yielding six relatively well–developed larval embryos (head capsules were visible), while the remaining four were undeveloped liquid.
A total of 366 larvae hatched successfully from the eggs at 07:00–14:00 during the dates 05–12 Jul. 2022. Spraying water onto the egg shells is one of the key stimuli for larval eclosion. Processionary behavior was observed during L1–4 of S. bouyeri (e.g., Fig.
Sinobirma bouyeri. A A cluster of fresh L1 (with ova and eggshells), dorsal view, scale bar = 6 mm. B Processionary L1 rebuilding the cluster on Lagerstroemia indica, dorsal view, scale bar = 5 mm. C A cluster of pre-molting L1 on Prunus cerasoides, dorsal view, scale bar = 6 mm. D A cluster of L1–2 resting on Salix babylonica, scale bar = 5 mm. E A cluster of L2 feeding on Coriaria nepalensis, dorsal view, scale bar = 10 mm. F A Pre-molting L2 moving and rebuilding their cluster on P. cerasoides, lateral view, scale bar = 5 mm. G A cluster of L3 feeding on P. cerasoides, dorsal view, scale bar = 10 mm. H A cluster of L4 resting on C. nepalensis, dorsal view, scale bar = 10 mm. I A cluster of L5 resting on the lower parts of the stems of C. nepalensis, dorsal-lateral views, scale bar = 10 mm.
Larvae of different instars and originating from different females aggregated regularly (e.g., Fig.
From L1, the larvae fed on leaves by starting from the edges, rather than gnawing a hole into the surface. They were not observed feeding on stems, except for a few L5. Larvae showed different degrees of the feeding behavior during day and night. The leaves of C. nepalensis are relatively small, but the larval groups could aggregate on the undersides of the leaves from L1 to early L4.
Starting with the late L4, due to their larger size, the strategy changed into clustered resting during the day and dispersed feeding at night. This is a circadian rhythm relates to negative phototaxis of the mature larvae. All 19 L5 in the C. nepalensis test group strictly formed a united cluster on the lower parts of the plant stems during the day, without any feeding and processionary activities (Fig.
Because the leaves of P. cerasoides are relatively larger and because of the uneven development of the 17 larvae in this test group, some larger L5 used to rest together on the lower stems during the day and to disperse to feed on leaves during the night. Sometimes 2–4 smaller larvae (during L5 or L6) aggregated on the undersides of leaves, but rarely fed by day (only about 0–2 times of feeding, one lasting less than 10 minutes); they mainly fed at night.
As an experiment, a stronger larva from the cauline larval cluster was selected and moved to a separate plant of P. cerasoides to record its feeding and defecation times over 24 hours (Fig.
24 hours (05 Sep. 2022) continuous observation of a single Sinobirma bouyeri L5 (Table S3), reared on Prunus cerasoides. Green bars = the time periods of larval feeding. Black triangles = the moments of larval defecation. Red line = temperature (°C). Blue line = humidity (RH%). Yellow line = illumination (Lux). The ordinate on the left is for polylines only (data sampling interval 10 minutes), 1 scale tick = 3°C = 8 RH% = 800 Lux. Scale bar at bottom visualizes illumination, with the darker parts representing night and the light gray day.
It is worth mentioning that the green parts of the mature larval integument appeared weakly fluorescent under ultraviolet excitation, while the black and yellow parts were non-fluorescent. In the tests, the fluorescence visible to human eyes were the strongest under 365 nm UV (Fig.
Scoli of L1–5 of the species had no apparent defensive function, and there was no irritant or urticating reaction upon contact with my skin. Most saturniid larvae rest with their thoracic legs lifted from the plants and hanging in the air, sometimes including the prolegs A3–4, but all larvae of S. bouyeri always firmly grasped the host plant with all legs and prolegs while at rest. The larvae would secrete a small amount of silk on the vegetation to anchor their crochets before entering each pre-molting period. The pre-molt larvae maintained the ability to move vigorously, and if necessary, they even changed the position of each individual within a cluster (e.g., Fig.
The midgut appeared brownish red externally in L1 that were raised on L. indica and P. cerasoides, but appeared bright green in L1 on S. babylonica and C. nepalensis. The final feces [frass] of all individuals that fed on C. nepalensis were dark green (Fig.
Sinobirma bouyeri. A–C Final feces of L5, reared on Prunus cerasoides (A), P. cerasoides (B) and Coriaria nepalensis (C), scale bars = 10 mm. D L5, burrowing into the soil after feeding had ended, lateral view, scale bar = 10 mm. E Entrance of larval borehole, covered with moss, scale bar = 5 mm. F Tunnel entrance after removing the moss in E, scale bar = 5 mm. G Fully tanned pupa ♀, ca. 9 cm from the upper surface of the moss-layer and its head is orienting upward to this surface, scale bar = 10 mm. H Freshly molted and incompletely tanned ♀ pupa, ca. 10 cm from the upper surface of the moss-layer, scale bar = 20 mm.
A total of 15 males and 19 females pupated in the soil at 6–12 cm depth (the distances from pupa to the upper surface of the moss-layer). The weights of pupae reared on P. cerasoides were 1.23–1.74 g for males (average: 1.61 g) and 1.53–2.27 g for females (average: 1.90 g), respectively. In contrast, those that fed on C. nepalensis weighed 1.56–2.15 g for males (average: 1.95 g) and 2.03–2.66 g for females (average: 2.32 g), respectively (Table S4).
From all rearings, only one natural tunnel was retained in its entirety, with the inside of it slightly collapsed from excavating pupae. The longitudinally sectioned tunnel was photographed after repairing it (Fig.
Each pupa was surrounded by a gap of ca. 1–3 mm between pupal shell and soil (Fig.
Unhatched ova of S. bouyeri were stored in a plastic zip lock bag at room temperature (ca. 19–24°C) from 25 Jul. to 3 Sep. 2022. A dead minute wasp found in this bag is the only egg parasitoid recorded for the genus Sinobirma so far:
Single ♀ wasp (Fig.
The topologies of the ML trees calculated in both MEGA X and IQ-TREE were exactly the same. The topological relationship is (((Saturniini + Attacini) + (Micragonini + Eochroini)) + (Urotini + Bunaeini)) + outgroup (Fig.
The evolutionary relationships of Sinobirma and its relatives have been discussed controversially in literature. When establishing the genus Maltagorea,
To elucidate the origin of Sinobirma further, this discussion is focused on comparing morphological and biological characteristics between Sinobirma bouyeri and genera that have been proposed as close relatives. Additional independent molecular evidence from mitochondrial DNA is also discussed.
At present, the putative sister genera of Sinobirma still lack microscopic morphological observations on ova for comparison with Sinobirma. The egg chorion of Pseudantheraea discrepans (Butler, 1878) shows a fine reticulation at 24x magnification (
Similarly to eggs, very little is known about the early larval instars of the relatives of Sinobirma. The L1 of S. malaisei appear almost indistinguishable from those of S. bouyeri as illustrated in
In the L5 of T. flavinata, the sclerotized parts (mainly the head capsule, prothoracic shield, anal shield, legs T1–3, lateral plates of prolegs A3–6 and A10, bases of scoli SV, L, SD, D and XD) are of similar colors near red-orange. In contrast, the same areas of fresh L5 of S. bouyeri are all bright yellow just after ecdysis (Fig.
The largest segments are always A3–4, for S. bouyeri L2–5, making the larva as a whole shaped cylindrical but slightly tend to fusiform. As mentioned above, when the larvae were in a physically relaxed state, the dorsal area of the junction zone between A1/A2 appeared to be the most sunken area in lateral view, especially in L2–5 (Fig.
The bases of the paired scoli D-III are medially fused on A8 in S. bouyeri. This character is also present in T. flavinata as described by
One noteworthy feature of S. bouyeri is the flattened A10 in lateral view of L1–5, with the posterior margins of the pair of lateral plates of the anal prolegs usually combined to form a minor arc outline in dorsal view. This means that the opening angle between the two anal prolegs is very flexible, whereas it is usually in a horizontal state (nearly straight line). This structure is presumably suitable for crawling and clustering on the smooth surfaces of the undersides of leaves.
Furthermore, the triangular anal shields of L4–5 of S. bouyeri are all drawn out to form a pointed posterior tip, a feature shared with the mature larvae of T. genoviefae (
For S. bouyeri, each scolus D-II on the anal shield bears 2 primary setae during L1–5. A similar trait had been known to occur in some other members of the tribe Urotini, but also in other African tribes (
The pupal shell of S. bouyeri has three pairs of dorsal thoracic tubercles of large sizes, and a very long, spiny cremaster on the tip of A10.
While multiple potential sister genera share the aforementioned morphological features with S. bouyeri, differences in structural detail exist between them. For examples, images in the above literature show that scoli D of T2–A9 appear spine-like and strongly elongated in the mature larva of P. discrepans, with lateral margins of the anal shield curved. Larvae of M. auricolor and similarly M. fusicolor (illustrated by
The trait of medially fused scoli D on A8 has been known to be shared by larvae of Tagoropsis spp., S. malaisei and S. bouyeri, but M. auricolor and P. discrepans hatch with a pair of scoli D on A8 that are completely separated from each other.
Mature larvae of U. wallengrenii and U. terpsichore do not have an elongated posterior tip of the anal shield, and the pupa of the former species has a posterior elevated crest in annular shape on A4–6. These characteristics also appear in the pupa of U. angulata (
Although the color combinations of the final larval instar of the above related African genera do not have similar patterns to S. bouyeri, coincidentally, the colors of the mature larva of the Australian Opodiphthera astrophela (Walker, 1855) are similar, especially in the painting in
Despite all the similarities and differences, further data from African species would be needed to identify which characters are informative to reconstruct a morphology-based phylogeny. At present, our knowledge of the above genera is incomplete, and especially detailed morphological and biological work involving ova, larvae and pupae are rare. Nevertheless,
Exploring the plants that Sinobirma accepted or rejected can provide insights into its ecological niche. Previously, only
This study tested host plant acceptance by S. bouyeri systematically. Plants completely rejected by the larvae of S. bouyeri came from the families Ericaceae, Malvaceae, Lauraceae, Betulaceae, Magnoliaceae, Pinaceae, Vitaceae and Santalaceae. Similarly, there were minute bite marks, but the larvae did not continue to feed and even starved to death when attempted to rear on Meliaceae, Rutaceae and Theaceae.
Altingiaceae seems to be a special case where within a group some larvae clearly accepted but some totally rejected the offered host plant, thereby separating two dinstict larval clusters in the rearing container. Ultimately, none of the larvae developed on this host. Similarly, S. bouyeri rejected two but fed one species within the family Fabaceae, but the accepted plant caused the caterpillars to die consecutively over several days. The same acceptance yet mortality pattern occurred also with Anacardiaceae, Fagaceae, Nyssaceae, Phyllanthaceae and Oleaceae. Even more problematic was the rearing on Sapindaceae and Ulmaceae, which resulted in all individuals of each larval group to die rapidly the same day.
Regrettably, no valid data were available for the group testing on Symplocaceae and it remains unknown whether the larvae of S. bouyeri can molt to L2 or even complete the whole larval stage. This family of plants is rarely reported as a host plant of saturniids, e.g., A. atlas was reported to feed on Symplocos paniculata in India (
Of all the tested host plants, only 5 families of plants were able to support the development of S. bouyeri larvae from L1 molting into L2. The least suitable plant was J. regia, as all larvae died soon after the first ecdysis. This result is consistent with the mortality of S. malaisei observed by
Of all the plants tested, C. nepalensis in the family Coriariaceae is the best host plant for S. bouyeri. There were no larval losses from hatching to the last larva burrowing into the soil, and the developmental duration was almost a month shorter than that of larvae fed on P. cerasoides (Table S1). As a shrub (Fig.
Of the genera that are closely related to Sinobirma, Tagoropsis occurs only on the mainland of Sub-Saharan Africa and was long known to feed on Sapindaceae. An early report by
Pseudantheraea is a polyphagous genus occurring in central-western Africa, feeding on multiple botanical families in the wild. Poga oleosa (Anisophylleaceae) and Uapaca guineenis (Phyllanthaceae) were recorded as natural hosts of P. discrepans in Gabon, while the genus Terminalia (Combretaceae) was accepted in captivity (
Maltagorea is restricted to Madagascar and lacks detailed preimaginal reports. Larvae of M. fusicolor have been known to feed in the wild on the tapia tree Uapaca bojeri (Phyllanthaceae) (
As mentioned above, a further seven African genera Urota, Pseudaphelia, Pselaphelia, Eudaemonia, Antistathmoptera, Usta and Parusta have been considered as relatives of Sinobirma to varying degrees in different works. According to the comprehensive catalogues of the host plants of Saturniidae by
More rigorous comparative conclusions could not be drawn as it wasn’t possible to test the host plants of all of the above African Saturniidae. Furthermore, it is uncertain whether records in literature resulted in larvae reaching pupation or could even sustain multiple generations. However, polyphagy is here proposed to be a shared trait of the closely related genera Tagoropsis, Pseudantheraea, Maltagorea and Sinobirma.
The natural habitat of S. bouyeri in China is recorded here as the Nyingchi area of the Tibet Autonomous Region, a prefecture-level city whose territory contains both northern and southern sides of the eastern Himalayas and the Yarlung Tsangpo River [upper Brahmaputra]. Bomê [Pome] and Mêdog [Metok] are both counties that belong to Nyingchi, as the type locality. The average annual rainfall of the former region exceeds 800 mm, largely in spring (>300 mm) and summer (>300 mm), with an average temperature of 0–2°C in winter and 16–18°C in summer (
The genera Tagoropsis, Pseudantheraea and Maltagorea are mainly forest and grassland dwellers (Fig.
Based on the oviposition behavior described in section 3.4.1, females of S. bouyeri may prefer to oviposit in the wild onto surfaces facing the sky (such as the uppersides of leaves or branches), as well as into narrow crevices or pits (such as cracks of stems). This would provide the eggs more exposure to rain and warmth within the understory that’s low in sunlight.
Comparing observations made for the L4–5 S. bouyeri larval groups reared on C. nepalensis and P. cerasoides (section 3.4.3), it appears that larval cluster size and location on the plant have an influence on the gregarious behaviour. For smaller larvae that inhabited the leaf undersides during the day, the more larvae in a cluster, the more stable the rhythmical feeding-resting behavior was. In contrast, larger larvae that typically clustered on lower stems during the day exhibited the most stable gregarious behaviour. These results are based on only a relatively small number of individuals and observations, and more rigorous experiments are needed in the future to further determine the regulatory role of other factors like light and pheromones in the circadian rhythm of larvae.
Pupation of the mature larvae in captivity was described in detail in section 3.4.4. In nature, soil tends to be substantially more dense and to include more rock particles and plant roots. Therefore, most larval S. bouyeri might only burrow to a soil depth of less than 10 cm naturally, but otherwise similarly to the results in section 3.4.4.
The above publications indicate that some species of the African genera Tagoropsis, Pseudantheraea and Maltagorea have two (or more) flights per year. In contrast, Asian Sinobirma is strictly univoltine (see introduction), which is probably an adaptation to the colder Himalayas, but may also correspond to seasonal metabolic rhythms of their natural host plants.
P. discrepans has long been known for its peculiar green pupa hanging in a loose cocoon amongst the vegetation (e.g.,
Considering the above larval characteristics, Tagoropsis is the closest genus to Sinobirma at the behavioral level. Some species of the two genera are known to have similar larval circadian rhythm and naked, subterranean pupae.
Larval fluorescence has rarely been reported for Saturniidae. Besides S. bouyeri,
The fluorescent green stripes of S. bouyeri L5 were conspicuous in daylight, which seemed to provide excellent camouflage in vegetation when larvae clustered at the inferior parts of the stems during the day — due to the rainy climate, Sub-Himalayan broad-leaved forest is extensively covered with moss, especially the understory.
Using a taxonomic key for the order Hymenoptera (
However, the topologies in these papers (Fig.
At first glance, the inclusion of the Himalayan genus Sinobirma in the otherwise exclusively African tribe Urotini might seem at odds from a biogeographic perspective and require discussion. Following the phylogeny of
Hypothesis I. A Gondwanan origin of the group’s ancestor, prior to India separating from Madagascar (land connection or dispersal across narrow straits still possible). After complete separation of India (straits too wide for dispersal), the ancestor present in India developed into a distinct lineage (Sinobirma) that arrived in Asia, whereas the individuals in Africa split into lineages on the mainland (Tagoropsis and Pseudantheraea) and Madagascar (Maltagorea).
Hypothesis II. After India had separated completely from Madagascar, the ancestor of Sinobirma originated from taxa in mainland Africa (Tagoropsis and Pseudantheraea) or Madagascar (Maltagorea), followed by expansion to Asia (Sinobirma) and extinction in Africa.
Hypothesis III. The common ancestor originated on the Eurasian Plate, or the insular India (completely separated from Madagascar), or formed after the two land masses collided, giving rise to the Asian lineage (Sinobirma) and dispersing to mainland Africa (Tagoropsis and Pseudantheraea) and finally Madagascar (Maltagorea).
Immature stages of the family Saturniidae make up the longest part of the lifecycle, and larval habitus and behavioral features are particularly influenced by evolutionary pressures linked to the biotopes they occur in. Firstly, the immatures of Pseudantheraea and Maltagorea each of features that are unique within the group of genera, while Tagoropsis and Sinobirma share fairly visible, similar characteristics, i.e., in morphology and biology of larvae and pupae. These shared features are unlikely to have evolved convergently, and the sharing of homologous characteristics indicates that the historical habitat of Sinobirma was probably more similar to the one of Tagoropsis.
Secondly, both Pseudantheraea and Tagoropsis occur on the African continent in adjacent or partially overlapping habitats (Fig.
Considering the extensive distribution of Urotini and its sister tribe Bunaeini in Africa (see section 4.6), these African taxa and Sinobirma seem unlikely to be of shared Asian origin, rendering hypothesis III unrealistic. The Himalayas have been central to the evolution of most Asian saturniid genera/subgenera except Perisomena Walker, 1855, i.e., the genera Actias Leach, 1815, Antheraea Hübner, 1819, Telea Hübner, 1819, Antheraeopsis Wood-Mason, 1886, Cricula Walker, 1855, Lemaireia Nässig & Holloway, 1988, Rinaca Walker, 1855, Cachosaturnia Naumann, Löffler & Nässig, 2012, Saturnia Schrank, 1802, Neoris Moore, 1862, Loepa Moore, 1859, Attacus Linnaeus, 1767, Archaeoattacus Watson, 1914, Samia Hübner, 1819, Rhodinia Staudinger, 1892, Solus Watson, 1913, Salassa and Aglia Ochsenheimer, 1810. These genera have all a wider subtropical and tropical Asian, temperate palearctic or even New World distribution. In contrast, Sinobirma is a relict taxon with a distribution restricted to the northeastern corner of the Indian plate.
This paper discussed the life history and related biological characteristics of the genus Sinobirma, leading to the really central questions of how and when Sinobirma separated phylogenetically and geographically from its closest relatives in Africa. Multiple characteristics strongly support hypothesis II (section 4.7), i.e., that the ancestor of Sinobirma arrived in Asia by dispersal, rather than by continental drift as favoured by
Relative to the other two genera, immature stages of Tagoropsis and Sinobirma share more morphological and biological similarities, which is here considered to be key for clarifying the dispersal history of the latter. However, this does not mean that Tagoropsis and Sinobirma are sister taxa in a phylogenetic sense, because it isn’t clear at present to what extent these traits are shared ancestral or derived characteristics.
The host preference experiment demonstrated that although larvae died quickly in L1 after feeding on some hosts, the feeding behavior of the early larva of the genus Sinobirma can be triggered by many different Himalayan plants within different families. This potential to exploit a broad range of plants might have enabled moths to expand their populations without the constraints caused by monophagy and the distribution of a specific host plant. Consequently, these larvae are well equipped to continuously discover and adapt to new, suitable host plants in natural environments in a relatively short time, as might be expected during dispersal. Considering that Tagoropsis, Pseudantheraea and Maltagorea all utilize a much broader range of host plants, this may indicate that their most recent common ancestor might have been polyphagous.
Before reaching today’s southeastern Himalayas, whether through Europe, the Middle East or both, the northwestern Indian subcontinent was obviously the logical dispersal route for the ancestors of Sinobirma. None of these areas is home to the four genera today, only a distantly related Usta species occurs on the dry Arabian Peninsula (
Genomic research by Rougerie et al. (preprint) demonstrated that Sinobirma dispersed from Africa to the Oriental region in the middle Miocene (ca. 14 Mya), whereas Maltagorea colonized Madagascar from the African continent at a similar time (ca. 12 Mya). According to
Rougerie et al. (preprint) already mentioned that the dispersals by Epiphora Wallengren, 1860, Eosia Le Cerf, 1911, and Argema Wallengren, 1858 occurred from Asia to the Africa (ca. 14 Mya), almost synchronous with the divergence of Sinobirma from its African relatives. This might mean that their ancestors all encountered a common historical event in the same region, most likely aridification. This might have increasingly restricted distributions to relatively wet areas, separating populations.
Opinions differ on when the Sahara and Arabian deserts formed.
In the superfamily Bombycoidea, another Sub-Himalayan taxon Tibetanja Naumann, Nässig & Rougerie, 2020 (Eupterotidae) may have the same distributional pattern and dispersal history as the saturniid genus Sinobirma. The former is probably the only Asian genus of the African subfamily Janinae (Eupterotidae) (
In any case, it is necessary to explore the immature characteristics of more members of the genera Tagoropsis, Pseudantheraea and Maltagorea, as well as of S. malaisei and S. myanmarensis to further refine our understanding of the evolution of the genus Sinobirma.
I am most sincerely grateful to Richard S. Peigler (University of the Incarnate Word, San Antonio) for his guidance and help in my studies of Saturniidae in recent years. He provided much literature and valuable advice, as well as editing the English for this article. Rodolphe Rougerie (Muséum National d’Histoire naturelle, Paris) is one of the few people who has personally traveled to the natural habitat of Sinobirma to study the genus, and I thank him for providing references and reviewing my manuscript. Andreas Zwick (Commonwealth Scientific and Industrial Research Organisation, Canberra) helped with advice and editing the manuscript. Michel J. Faucheux (Faculté des Sciences et des Techniques, Nantes) shared with me knowledge about sensilla. Finally, special thanks go to Yanqun Liu (Shenyang Agricultural University, Shenyang) and Dasong Chen (Institute of Zoology, Guangdong Academy of Science, Guangzhou), who assisted in genomic data analyses and reviewed the relevant paragraphs.
Tables S1–S3, S5, S6
Data type: .xlsx
Explanation notes: Table S1. Individual numbers of Sinobirma bouyeri in different developmental stages, fed on Coriaria nepalensis (group A, in green bars) and Prunus cerasoides (group B, in red bars), respectively. — Table S2. Environmental monitoring data for the habitat of Sinobirma bouyeri (Mêdog County, Tibet, 2134 m) — Table S3. Circadian rhythm of Sinobirma bouyeri L5. — Table S5. Taxonomic checklist of Sinobirma and its close relatives. — Table S6. Inventory of DNA sequences used in this paper.
Table S4
Data type: .pdf
Explanation notes: Pupal data of Sinobirma bouyeri raised on Coriaria nepalensis and Prunus cerasoides.
File S1
Data type: .mov
Explanation notes: Gregarious behavior of fresh Sinobirma bouyeri L1.