Developmental cost of leg-regenerated Coccinella septempunctata (Coleoptera: Coccinellidae)

PLOS ONE, Jan 2019

As larval cannibalism is common under intensive rearing conditions, leg regeneration can help ladybugs adapt to the competitive environment, but whether the leg regeneration leads to side effects on development remains unclear. To analyze the potentially developmental cost of leg regeneration, the developmental period and weight of leg-regenerated Coccinella septempunctata were studied in the laboratory. The results showed that, when the time intervals between the emergency of 4th-instar larva and leg amputation increased, the developmental period of leg-regenerated 4th-instar larvae was gradually prolonged. Significantly developmental delay were also examined at prepupal and pupal stages, and various timings of leg amputation affected the periods of leg-regenerated prepupae/pupae similarly. After the leg was amputated at different larval instars, the developmental delay only occurred at the larval instar when the leg was amputated, whereas other larval instars failed to be extended, and the developmental periods of leg-regenerated prepupae/pupae were affected similarly by the instars of leg amputation. Developmental delays possibly resulted in more consumption by leg-regenerated larvae, and then weight gains at prepupal/pupal stages, but different larval instars of leg amputation affected the weight gain similarly. Both the developmental delay (at 4th-instar larval, prepupal and pupal stages) and weight gain (at pupal and adult stages) in complete/bilateral amputation were longer or greater than those in half/unilateral amputation. However, the thoracic locations of leg amputation impacted the developmental delay and weight gain similarly. Our study indicates that although leg regeneration triggers the developmental cost decreasing the competitive superiority or agility, C. septempunctata larvae still choose to completely regenerate the leg to adapt to complex environments. Thus, in order to remain competitive at adult stages, leg-impaired larvae may make an investment tradeoff between leg regeneration and developmental cost.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0210615&type=printable

Developmental cost of leg-regenerated Coccinella septempunctata (Coleoptera: Coccinellidae)

January Developmental cost of leg-regenerated Coccinella septempunctata (Coleoptera: Coccinellidae) Pengxiang Wu 0 1 2 Fengming Wu 0 1 2 Shuo Yan 0 1 2 Chang Liu 1 2 Zhongjian Shen 0 1 2 Xiaofei Xiong 0 1 2 Zhen Li 0 1 2 Qingwen Zhang 0 1 2 Xiaoxia LiuID 0 1 2 0 Department of Entomology, China Agricultural University , Beijing , China , 2 Entomology and Nematology Department, University of Florida , Gainesville, FL , United States of America 1 Editor: Allah Bakhsh, Nigde Omer Halisdemir University , TURKEY 2 a Current address: Institute of Zoology, Chinese Academy of Sciences , Beijing , China ?b Current address: University of Chinese Academy of Sciences , Beijing , China - Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This study was funded by the National Key Research and Development program of China (2017YFD0201900 to XL). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. As larval cannibalism is common under intensive rearing conditions, leg regeneration can help ladybugs adapt to the competitive environment, but whether the leg regeneration leads to side effects on development remains unclear. To analyze the potentially developmental cost of leg regeneration, the developmental period and weight of leg-regenerated Coccinella septempunctata were studied in the laboratory. The results showed that, when the time intervals between the emergency of 4th-instar larva and leg amputation increased, the developmental period of leg-regenerated 4th-instar larvae was gradually prolonged. Significantly developmental delay were also examined at prepupal and pupal stages, and various timings of leg amputation affected the periods of leg-regenerated prepupae/pupae similarly. After the leg was amputated at different larval instars, the developmental delay only occurred at the larval instar when the leg was amputated, whereas other larval instars failed to be extended, and the developmental periods of leg-regenerated prepupae/pupae were affected similarly by the instars of leg amputation. Developmental delays possibly resulted in more consumption by leg-regenerated larvae, and then weight gains at prepupal/pupal stages, but different larval instars of leg amputation affected the weight gain similarly. Both the developmental delay (at 4th-instar larval, prepupal and pupal stages) and weight gain (at pupal and adult stages) in complete/bilateral amputation were longer or greater than those in half/unilateral amputation. However, the thoracic locations of leg amputation impacted the developmental delay and weight gain similarly. Our study indicates that although leg regeneration triggers the developmental cost decreasing the competitive superiority or agility, C. septempunctata larvae still choose to completely regenerate the leg to adapt to complex environments. Thus, in order to remain competitive at adult stages, legimpaired larvae may make an investment tradeoff between leg regeneration and developmental cost. Introduction Regeneration is a process of regrowing or renovating injured tissues/cells in organisms [ 1,2 ], and the in-depth study of regeneration may contribute to technical improvements in repairing damaged human organs [3]. Epimorphosis observed in both vertebrate and invertebrate is the tissue reestablishment of lost parts via cell multiplication [ 4,5 ]. Rebuilding impaired appendages is common across many taxonomic groups such as malacostracan crustaceans [6] and insects [ 7,8 ], contributing to researches in various respects [ 9 ] containing genetic, cellular, tissue, organic and organismal mechanisms. Leg regeneration in insects has been studied in at least 36 genera of 11 orders, including Blattaria, Periplaneta americana [ 10 ], Leucophaea maderae [ 11 ], Eupolyphaga sinensis Walker [ 12 ], Phasmida, Sinophasma spp. [ 13 ], Orthoptera, Acheta domestica [ 14 ], Lepidoptera, Galleria mellonella [ 15 ], Odonata, Ischnura cervula [ 16 ], Dictyoptera, Blattella germanica [17], Triatominae, Rhodnius prolixus [18], Heteroptera, Onco peltus fasciatus [ 19 ], Coleoptera [ 20,21,22 ], Tribolium castaneum [ 23 ]. Numerous studies associated with regeneration are also reported in hemimetabolous insects such as cockroaches [ 24,25 ] and crickets [ 26,27 ]. Leg regeneration helps insects adapt to competitive environments, but also causes developmental costs. Different forms of organ/tissue damage cause a systemic reaction of insects, and thus extend developmental periods. Mini-incisions to the integument of Galleria extend the larval duration by nearly a day [ 28 ], and leg amputations also lead to developmental delays of Blattella and Periplaneta [ 29,30,31,32 ]. The regeneration of injured legs influences the molt cycle of insects, resulting in the molting delay [ 33,34,35,36,37,38,39,40,41,42,43 ]. Many insects have a capability to heal impaired legs through localized cell proliferation [ 44 ]. Insulin-like peptides secreted by impaired imaginal tissues of Drosophila act as a signal inhibiting ecdysteroid production [ 45,46,47,48,49,50,51 ], causing developmental delays [ 52,53,54 ]. The development may be suspended until the injured cells/tissues are regrown and then intact morphologies appear [ 55,56 ]. Moreover, the pupal stage is also affected by the damage, larval Drosophila injured in 48?84 hours delays the pupariation [ 57,58 ]. Ecdysteroids can control the period of developmental transitions including larval-larval, larval-pupal and pupal-adult molts [ 59,60,61 ]. The degree of developmental delay depends on two potential factors: the amount of impaired tissue/cell and the developmental stage when damage occurs [ 62,63,64,65,66 ]. Besides delays at larval stages, the pupariation delay is also positively correlated with the amount of injured larval tissues/cells [ 67,68 ]. Similarly, after fragments of wing imaginal discs are implanted into Ephestia larvae, the fragments regenerate completely, leading to pupariation delays [41]. Moreover, injures at different developmental timings have different effects [ 56,60,61,62 ]. For example, imaginal disc fragments are transplanted into Ephestia at various larval stages, triggering different degrees of developmental delay [42]. Developmental delays make Harmonia axyridis invest more nutrient resources into regeneration, and increased consumption results in weight gains [ 21 ]. Under intensive rearing conditions, losing a leg is common for coccinellid larvae due to cannibalism. Although lost legs caused by cannibalism could be regenerated, the development of ladybugs may be affected. Thus in the current study, the developmental cost of leg-regenerated Coccinella septempunctata was examined. Our goals in this study were to determine: 1) whether the leg amputation at different timings of 4th-instar caused the developmental delay of leg-regenerated ladybugs. 2) Whether the factors containing the instar, site, thoracic location and amount of leg amputation influenced the developmental period and weight of legregenerated ladybugs. 2 / 14 Materials and methods Insects Ladybugs C. septempunctata were taken from our laboratory colony (Laboratory of Integrated Pest Management, China Agricultural University, Beijing, China). Larvae were kept in plastic containers (7 cm ? 4.5 cm ? 8 cm), reared with fresh bean aphids (Acyrthosiphon pisivorum) under the condition of a constant temperature of 25 ? 1?C, RH = 60?70% and a photoperiod of 16: 8 (L: D) under the light intensity of 600 lux. Effect of leg amputation at different timings of 4th-instar on the developmental period of leg-regenerated ladybugs To evaluate whether timings of leg amputation impacted development periods of leg-regenerated ladybugs, larvae at the 4th-instar rather than other instars were selected due to the longer duration. Zero-, 0.5-, 1-, 1.5-, 2-, 2.5-, 3-, 3.5- or 4 days after the 4th-instar larva emerged, its left-middle leg was amputated at the base of the tibia (half amputation), so each group contained 9 treatments. After anesthetization, the larva was placed on a double-sided tape, and the leg was amputated using a pair of micro-scissors. Then the leg-amputated larvae were held and fed in the same conditions as mentioned above. The 4th-instar larval, prepupal and pupal periods were recorded. Emerging adults were tested by microscopy to determine whether the amputated leg was regenerated again (the lost part reappeared). Moreover, ladybugs without any treatments were regarded as control. Each treatment was replicated three times simultaneously, and each replication included 20 ladybugs (male: female = 1: 1). Effects of instar, site, thoracic location and amount of leg amputation on the developmental period and weight of leg-regenerated ladybugs To analyze the factors influencing the developmental period and weight of leg-regenerated ladybugs, 1) the left-middle leg of larvae in three instars (2nd-, 3rd- or 4th-instar) was amputated at the base of the tibia (since 1st-instar larvae exhibited high mortality rates after leg amputation); 2) the left-middle leg of 4th-instar larvae was amputated at the base of the tibia (half amputation) or coxa (complete amputation); 3) the leg of 4th-instar larvae was half amputated at 3 thoracic locations (fore-, mid-, or hind leg); 4) the left-middle leg of 4th-instar larvae was half amputated in different amounts (unilateral or bilateral amputation) (Fig 1). Developmental periods of leg-regenerated larvae, prepupae and pupae were recorded, and the leg-regenerated pupae and adults were weighted using analytical balance (BS124S, Sartorius, Goettingen, Germany). Ladybugs without any treatments were regarded as control. Each treatment contained 20 ladybugs (male: female = 1: 1) and was replicated for three times simultaneously. Statistical analysis Descriptive statistics were given as the mean values and standard errors of the mean. Differ ences in developmental periods or weights between two treatments were examined using independent t-tests. Other data were analyzed using one-way ANOVA with the post hoc Tukey?s honest test of significance at the 5% level of statistical significance. All statistical analyses were conducted using the SPSS 20.0 software (IBM, Armonk, NY). 3 / 14 Fig 1. Complete amputation: The larval leg of C. septempunctata was amputated at the base of the coxa. Half amputation: the larval leg was amputated at the base of the tibia. Unilateral amputation: one larval leg was amputated. Bilateral amputation: a pair of legs was amputation. Scale bars equal 1000 ?m. Developmental periods of leg-regenerated 4th-instar larvae were prolonged progressively when the leg was amputated from day 0 to day 4, and almost all 4th-instar larval periods of leg-regenerated ladybugs significantly longer than that of control (F9, 38 = 155.556, P < 0.001; Fig 2A). Various timings of leg amputation affected developmental periods of leg-regenerated prepupae/pupae similarly, but both leg-regenerated prepupae (F9, 20 = 2.895, P = 0.014; Fig 2B) and pupae (F9, 20 = 2.831, P = 0.025; Fig 2C) delayed development significantly compared to normal individuals after the leg was amputated at the different timings. 4 / 14 Fig 2. Mean (? SE) developmental periods (d) of leg-regenerated ladybugs at various stages after the leg was amputated at different timings of 4th-instar. A. Fourth instar larva; B. Prepupa; C. Pupa. Different letters indicate significant differences among the treatments (Tukey?s HSD, P < 0.05). Effects of instar, site, thoracic location and amount of leg amputation on the developmental period and weight of leg-regenerated ladybugs Developmental period. After the leg was amputated at various larval instars, only the larval instar when the leg was amputated was significantly extended. Compared to normal periods, developmental periods of leg-regenerated 2nd-, 3rd- and 4th-instar larvae were prolonged significantly when the leg was amputated at the 2nd- (F3, 8 = 8.373, P = 0.008), 3rd- (F3, 8 = 16.265, P = 0.001) and 4th- (F3, 8 = 26.821, P < 0.001) instars, respectively. Moreover, the developmental periods of leg-regenerated prepupa and pupa were impacted similarly by the instars of leg amputation, and both of them were extended significantly compared to normal periods (prepupa, F3, 8 = 7.357, P = 0.011; pupa, F3, 8 = 4.279, P = 0.044; Fig 3A). 5 / 14 Fig 3. Mean (? SE) developmental periods (d) of leg-regenerated ladybugs at 4th-instar larval, prepupal and pupal stages. A. Results in amputation at various larval stages, i.e., the 2nd-, 3rd- or 4th instar, together with CK (normal developmental duration); B. Results in half and complete amputations; C. Results in amputations at various thoracic locations (fore-, mid- or hind leg); D. Results in unilateral and bilateral amputations. Different letters indicate significant differences among the treatments (Tukey?s HSD, P < 0.05). Asterisks indicate significant differences between two treatments (independent t-test, P < 0.05; P < 0.01). Developmental delays of leg-regenerated 4th-instar larvae (t4 = 3.551, P = 0.024), prepupae (t4 = 6.283, P = 0.003) or pupae (t4 = 2.895, P = 0.044) in complete amputation were significantly longer than those in half amputation (Fig 3B). However, the developmental periods at 4th-instar larval (F2, 6 = 0.102, P = 0.904), prepupal (F2, 6 = 0.082, P = 0.922) and pupal (F2, 6 = 0.048, P = 0.954) stages were affected similarly by thoracic locations of leg amputation, i.e., the fore-, mid- or hind leg (Fig 3C). Both bilateral and unilateral amputations caused developmental delays of leg-regenerated ladybugs, and the 4th-instar larval (t4 = 3.077, P = 0.037), prepupal (t4 = 3.202, P = 0.033) and pupal (t4 = 3.141, P = 0.035) periods in bilateral amputation were significantly longer than those in unilateral amputation (Fig 3D). 6 / 14 Weight. When the leg of ladybugs was amputated at various larval instars, the weights of leg-regenerated pupae/adults were impacted similarly by the instars of leg amputation, and both the leg-regenerated pupae (F3, 8 = 11.696, P = 0.003) and adults (F3, 8 = 9.774, P = 0.005) gained weights significantly compared to normal individuals (Fig 4A). Weight gains of legregenerated pupae (t4 = 4.26, P = 0.013) or adults (t4 = 2.939, P = 0.042) in complete amputation were significantly greater than those in half amputation (Fig 4B). Nevertheless, pupal (F2, 6 = 0.033, P = 0.967) or adult (F2, 6 = 0.025, P = 0.975) weights were affected similarly among various thoracic locations of leg amputation (Fig 4C). Leg-regenerated pupae (t4 = 4.732, P = 0.009) or adults (t4 = 2.808, P = 0.048) gained greater weights in bilateral amputation compared to those in unilateral amputation (Fig 4D) (All data from figures are provided in S1 Fig 4. Mean (? SE) weights (mg) of leg-regenerated ladybugs at pupal and adult stages. A. Results in amputations at the 2nd-, 3rd- or 4th instar larval stage, together with CK (normal weight); B. Results in half and complete amputations; C. Results in amputations at various thoracic locations (fore-, mid- or hind leg); D. Results in unilateral and bilateral amputations. Different letters indicate significant differences among the treatments (Tukey?s HSD, P < 0.05). Asterisks indicate significant differences between two treatments (independent t-test, P < 0.05; P < 0.01). 7 / 14 Discussion Developmental delay of leg-regenerated ladybugs Some species such as crab and scolopendra shorten developmental periods during leg regeneration [ 12,69 ], whereas many species including Drosophila, Ephestia and Galleria delay development after the leg was impaired [ 15,31,45,55,61,70 ]. Since larval cannibalism is frequent in intensive rearing systems, regenerating lost legs is common for C. septempunctata to adapt to the competitive environment, but in the meantime the normal development of this beneficial species is impacted. Developmental delays of leg-regenerated ladybugs were observed when the leg was amputated at various timings of 4th-instar, and developmental periods of legregenerated 4th-instar larvae were gradually prolonged with increased intervals between the emergence of 4th-instar larva and leg amputation, suggesting that development might be suspended until the damaged leg was regrown [ 55,56 ], so the timing of leg amputation impacted the degree of developmental delay [ 60,61 ]. It is also found that in Blattella germanica and Periplaneta americana, the leg amputation delayed the subsequent molt until wound healing and complete regeneration of the leg [ 30,68 ]. Insulin-like peptides secreted by damaged tissues act as a signal inhibiting ecdysteroid production, impacting normal larval-larval molts [ 51,52 ]. However, developmental delays were also tested at subsequently prepupal and pupal stages, implying that ecdysteroid controlled not only larval-larval molts but also larval-pupal molts [60,61]. Developmental period and weight of leg regenerated ladybugs are affected by the instar, site and amount of leg amputation When the leg was amputated at different larval instars, the obvious prolongation was only detected at the larval instar when leg amputation occurred, whereas other larval instars were not affected, indicating that the ecdysteroid might independently control molt cycle in each larval instar, causing that the developmental delay in each larval instar was independently impacted by leg amputation [ 71,72 ]. Furthermore, the degree of developmental delay at subsequently prepupal and pupal stages was affected similarly by larval instars of leg amputation. The consumption ratio of leg-regenerated/normal larvae was 1.103 (Wu unpublished data), so development delays might increase consumption by leg-regenerated larvae. Thus at a later stage, the leg-regenerated pupae and adults also significantly gained weights after the leg was amputated at different larval stages, further indicating extended time might be spent accumulating resources for leg regeneration and growth [9]. But on the other hand, weight gains may decrease the agility of ladybugs, damaging the competitive ability. Weight gains can be examined not only in insects, but also in other arthropods such as cellar spiders Holocnemus pluchei [ 73 ] and American lobster Homarus americanus [ 74 ]. The degree of developmental delays depends on not only the developmental stage of leg amputation, but also the amount of impaired tissues or cells [ 62,63,64 ]. In Periplaneta and Blattella, the amputation of a second leg causes an extra delay after a single leg is amputated [ 29,30,31,32,68 ]. Compared to half or unilateral amputation, more tissues are damaged in complete or bilateral amputation, so more time is spent on leg regeneration. Thus, developmental delays of leg-regenerated 4th-instar larvae, prepupae and pupae in complete/bilateral amputation were longer than those in half/unilateral amputation. Moreover, the degree of the developmental delays was impacted similarly among thoracic locations of leg amputation. Besides leg-amputation treatment, X-irradiation, ethyl methanesulfonate treatment and electromagnetic field also support the notion that the extent of delay is positively correlated with the amount of injured cells or tissues [46,60,61,65]. More damaged cells or tissues lead to 8 / 14 Fig 5. Regeneration of fore-, mid- or hind legs of C. Septempunctata adults after the legs bilaterally amputated at 4th-instar larval stages. Phenotypes after half amputation (A) and complete amputation (C) are shown. In the two columns on the right, B and D are color-level inversion images of the leg segments highlighted, both partial regeneration (red mark) and complete regeneration (aqua mark) are shown. Each scale bar equals 500 ?m. longer developmental delays, causing more consumption. Thus, similar to developmental delays, weight gains of leg-regenerated pupae and adults in complete/bilateral amputation were greater than those in half/unilateral amputation. Asymmetry of leg regeneration after bilateral amputation After fore-, mid- or hind legs were bilaterally amputated, asymmetric phenotypes were observed. Two leg-regenerated phenotypes were detected in both half and complete amputations: 1) partial regeneration, leg was regenerated, but some segments were not regenerated, or were regenerated but were fused together (aqua marks of the leg segments highlighted), and significantly shortened segments were mainly detected at the distal tibia and tarsus; 2) complete regeneration, legs were regenerated with normal segments (red marks of the leg segments highlighted) (Fig 5). In a somite, the nutrition supplying the regeneration of bilateral legs via hemolymph was uneven [ 75 ], possibly leading to non-consistent sizes of regenerated legs. Potential investment tradeoff between leg regeneration and developmental cost The leg regeneration triggered by cannibalism is common for coccinellid larvae in intensive rearing systems, but the mechanism of developmental delay and weight gain caused by leg regeneration remains unclear [76,77]. After leg amputation, the developmental cost of leg regeneration may decrease the competitive superiority and predatory agility of coccinellid 9 / 14 larvae. What is worse, physical lesions may cause mutations during leg regeneration, disrupting cell multiplication and then triggering systematic delays [ 78,79 ]. Although developmental costs of leg regeneration cause negative effects, C. septempunctata larvae still choose to regenerate the lost leg completely to adapt to competitive environments. After larval cannibalism, leg-damaged ladybugs may tend to make an investment tradeoff between structural recovery and developmental cost, and this investment selection is essential to remaining competitive at the adult stage. Supporting information S1 Table. Data of figures used in this study. (XLSX) Acknowledgments ing the paper. Author Contributions We thank Xuan Wang, Yanjun Liu and Yuhui Yang for reviewing, commenting and improv Conceptualization: Pengxiang Wu, Qingwen Zhang. Data curation: Pengxiang Wu, Fengming Wu, Xiaofei Xiong. Formal analysis: Pengxiang Wu, Shuo Yan. Funding acquisition: Qingwen Zhang, Xiaoxia Liu. Investigation: Pengxiang Wu, Fengming Wu, Zhongjian Shen. Methodology: Pengxiang Wu, Shuo Yan, Zhen Li. Project administration: Xiaoxia Liu. Resources: Qingwen Zhang, Xiaoxia Liu. Software: Shuo Yan, Xiaofei Xiong, Zhen Li. Validation: Qingwen Zhang, Xiaoxia Liu. Visualization: Pengxiang Wu. Writing ? original draft: Pengxiang Wu, Shuo Yan, Zhen Li. Writing ? review & editing: Pengxiang Wu, Shuo Yan, Chang Liu, Xiaoxia Liu. 10 / 14 11 / 14 38. Woods DF, Bryant PJ (1989) Molecular cloning of the lethal (1) discs large-1 oncogene of Drosophila. Dev Biol 134: 222?235. http://dx.doi.org/10.1016/0012-1606(89)90092-4 PMID: 2471660 12 / 14 13 / 14 1. Gui JF , Yi MS ( 2002 ) Developmental Biology , Science Press, Beijing, China. 154 pp. 2. Kumar A , Gates PB , Brockes JP ( 2007 ) Positional identity of adult stemcells in salamander limb regeneration . C R Biol 330 : 485 - 490 . https://doi.org/10.1016/j.crvi. 2007 . 01 .006 PMID: 17631442 3. Marsh JL , Theisen H ( 1999 ) Regeneration in insects . Semin Cell Dev Biol 10 : 365 - 375 . https://doi.org/ 10.1006/scdb. 1999 .0323 PMID: 10497093 4. Endo T , Bryant SV , Gardiner DM ( 2004 ) A stepwise model system for limb regeneration . Dev Biol 270 : 135 - 145 . https://doi.org/10.1016/j.ydbio. 2004 . 02 .016 PMID: 15136146 5. Shah M , Namigai E , Suzuki Y ( 2011 ) The role of canonical Wnt signaling in leg regeneration and metamorphosis in the red flour beetle Tribolium castaneum . Mech Dev 128 : 342 - 400 . https://doi.org/10. 1016/j.mod. 2011 . 07 .001 PMID: 21801833 6. Shock BC , Foran CM , Stueckle TA ( 2009 ) Effects of salinity stress on survival, metabolism, limb regeneration, and ecdysis in Uca pugnax . J Crustac Biol 29 : 293 - 301 . https://doi.org/10.1651/ 08 - 2990 .1 Wolpert L ( 2011 ) Positional information and patterning revisited . J Theor Biol 269 : 359 - 365 . https://doi. org/10.1016/j.jtbi. 2010 . 10 .034 PMID: 21044633 8. Tan LF , Zhao Y , Lei CL . 2013 . Development and integrality of the regeneration leg in Eupolyphaga sinensis . B Insectol 66 : 173 - 180 . URL: https://www.cabdirect.org/cabdirect/abstract/20133416547 PMID: 20133416547 9. Maginnis TL ( 2006 ) The cost of autotomy and regeneration in animals: a review and framework for future research . Behav Ecol 17 : 857 - 872 . https://doi.org/10.1093/beheco/arl010 10. Bodenstein D ( 1957 ) Studies on nerve regeneration in Periplaneta americana . J Exp Zool 136 : 89 - 115 . https://doi.org/10.1002/jez.1401360107 PMID: 13513959 11. Bohn H ( 1974 ) Extent and properties of the regeneration field in the larval legs of cockroaches (Leucophaea maderae) . J Embryol Exp Morphol 32 : 81 - 98 . http://dev.biologists.org/content/32/1/81.articleinfo PMID: 4452835 12. Tan LF , Zhu F , Liu J , Zhou XM , Lei CL ( 2004 ) Leg regeneration in Eupolyphaga sinensis (Blattodea: Corydiidae) . Acta Entomol Sin 47 : 719 - 724 . Chinese. 13. Chen SC , Chen PC ( 1999 ) A study on the regeneration of artus in genus Sinophasma gu?nther . Acta Entomol Siles 42 : 159 - 165 . Chinese. 14. Maleville A , Reggi M ( 1981 ) Influence of leg regeneration on ecdysteroid titres in Acheta larvae . J Insect Physiol 27 : 35 - 40 . https://doi.org/10.1016/ 0022 - 1910 ( 81 ) 90029 - 9 15. Madhavan K , Schneiderman HA ( 1969 ) Hormonal control of imaginal disc regeneration in Galleria mellonella (Lepidoptera) . Biol Bull 137 : 321 - 331 . http://dx.doi.org/10.2307/1540104 16. Parvin DE , Cook PJ ( 1968 ) Regeneration of appendages in damselflies . Ann Entomol Soc Am 61 : 784 - 785 . https://doi.org/10.1093/aesa/61.3. 784 17. O 'farrell AF , Stock A ( 1953 ) Regeneration and the moulting cycle in Blattella germanica L. I. Single regeneration initiated during the first instar . Aust J Exp Biol 6 : 485 - 500 . https://doi.org/10.1071/ BI9530485 PMID: 13093536 18. Knobloch CA , Steel C ( 1988 ) Interactions between limb regeneration and ecdysteroid titres in last larval instar Rhodnius prolixus (Hemiptera) . J Insect Physiol 34 : 507 - 514 . https://doi.org/10.1016/ 0022 - 1910 ( 88 ) 90192 - 8 19. Shaw VK , Bryant PJ ( 1974 ) Regeneration of appendages in the large milkweed bug, Oncopeltus fasciatus . J Insect Physiol 20 : 1847 - 1857 . https://doi.org/10.1016/ 0022 - 1910 ( 74 ) 90214 - 5 PMID: 4415516 20. Wu PX , Xiong XF , Li Z , Yan S , Liu XX , Zhang QW ( 2015 ) Developmental continuity between larval and adult leg patternings in Coccinella septempunctata (Coleoptera: Coccinellidae) . Fla Entomol 98 : 193 - 199 . https://doi.org/10.1653/024.098.0133 21. Wang S , Tan XL , Michaud JP , Shi ZK , Zhang F ( 2015 ) Sexual selection drives the evolution of limb regeneration in Harmonia axyridis (Coleoptera: Coccinellidae) . Bull Entomol Res 105 : 245 - 252 . https:// doi.org/10.1017/S0007485315000036 PMID: 25632883 22. Saxena S , Mishra G , Omkar ( 2016 ). Does regeneration ability influence reproductive fitness in Menochilus sexmaculatus, (Coleoptera: Coccinellidae)? . J Asia-Pac Entomol 19 : 829 - 834 . https://doi.org/ 10.1016/j.aspen. 2016 . 07 .012 23. Alison KL , Christie CS , Elaine RK , Yuichiro S ( 2013 ) Developmental coupling of larval and adult stages in a complex life cycle: insights from limb regeneration in the flour beetle, Tribolium castaneum . Evo Devo 4 : 2 - 17 . https://doi.org/10.1186/2041-9139-4-20 PMID: 23826799 24. Truby PR ( 1983 ) Blastema formation and cell division during cockroach limb regeneration . J Embryol Exp Morpholog 75 : 151 - 164 . https://www.ncbi.nlm.nih.gov/pubmed/6886608 PMID: 6886608 25. Tanaka A , Ohtake-Hashiguchi M , Ogawa E ( 1987 ) Repeated regeneration of the German cockroach legs . Growth 51 : 282 - 300 . https://www.ncbi.nlm.nih.gov/pubmed/3440526 PMID: 3440526 26. Lakes R , Mucke A ( 1989 ) Regeneration of the foreleg tibia and tarsi of Ephippiger ephippiger (Orthoptera: Tettigoniidae) . J Exp Zool 250 : 176 - 187 . https://doi.org/10.1002/jez.1402500209 27. Li H , Zhang XH , Na J ( 2007 ) The hind leg regeneration in the nymphs of Gryllus bimaculata . Chin Bull Entomol 44 : 419 - 422 . Chinese. 28. Mala J , Sehnal F , Kumaran AK , Granger NA ( 1987 ) Effects of starvation, chilling, and injury on endocrine gland function in Galleria mellonella . Arch Insect Biochem Physiol 4 : 113 - 128 . http://dx.doi.org/ 10.1002/arch.940040205 29. Kunkel JG ( 1977 ) Cockroach molting . II. The nature of regeneration-induced delay of molting hormone secretion . Biol Bull 153 : 145 - 162 . http://dx.doi.org/10.2307/1540698 PMID: 889943 30. O 'farrell A , Stock A ( 1954 ) Regeneration and the Moulting Cycle in . Blattella Germanica L. III. Successive Regeneration of Both Metathoracic Legs . Aust J Biol Sci 7 : 525 - 536 . https://doi.org/10.1071/ BI9540525 PMID: 13229848 31. Pohley J ( 1959 ) Experimentelle Beitra?ge zur Lenkung der Organentwicklung, des Ha?utungsrhythmus und der Metamorphose bei der Schabe Periplaneta americana L. . Dev Genes Evol 151 : 323 - 380 . http://dx.doi.org/10.1007/BF00577774 PMID: 28354209 32. Stock A , O'farrell AF ( 1954 ) Regeneration and the moulting cycle in Blattella germanica L. II. Simultaneous regeneration of both metathoracic legs . Aust J Biol Sci 7 : 302 - 307 . http://dx.doi.org/10.1071/ BI9540302 PMID: 13219037 33. Stieper BC , Kupershtok M , Driscoll MV , Shingleton AW ( 2008 ) Imaginal discs regulate developmental timing in Drosophila melanogaster . Dev Biol 321 : 18 - 26 . https://doi.org/10.1016/j.ydbio. 2008 . 05 .556 PMID: 18632097 34. Smith-Bolton RK , Worley MI , Kanda H , Hariharan IK ( 2009 ) Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc . Dev Cell 16 : 797 - 809 . https://doi.org/10.1016/j.devcel. 2009 . 04 .015 PMID: 19531351 35. Gateff E , Schneiderman HA ( 1974 ) Developmental capacities of benign and malignant neoplasms of Drosophila . Dev Genes Evol 176 : 23 - 65 . https://doi.org/10.1007/BF00577830 PMID: 28304815 36. Stewart M , Murphy C , Fristrom JW ( 1972 ) The recovery and preliminary characterization of X chromosome mutants affecting imaginal discs of Drosophila melanogaster . Dev Biol 27 : 71 - 83 . http://dx.doi. org/10.1016/ 0012 - 1606 ( 72 ) 90113 - 3 PMID: 4621757 37. Bryant PJ ( 1971 ) Regeneration and duplication following operations in situ on the imaginal discs of Drosophila melanogaster . Dev Biol 26 : 637 - 651 . http://dx.doi.org/10.1016/ 0012 - 1606 ( 71 ) 90146 - 1 PMID: 5002603 39. Martin P , Martin A , Shearn A ( 1977 ) Studies of l(3)c43hs1 a polyphasic, temperature-sensitive mutant of Drosophila melanogaster with a variety of imaginal disc defects . Dev Biol 55 : 213 - 232 . http://dx.doi. org/10.1016/ 0012 - 1606 ( 77 ) 90168 - 3 PMID: 402295 40. Bryant PJ , Schubiger G ( 1971 ) Giant and duplicated imaginal discs in a new lethal mutant of Drosophila melanogaster . Dev Biol 24 : 233 - 263 . http://dx.doi.org/10.1016/ 0012 - 1606 ( 71 ) 90097 - 2 PMID: 4994924 41. Rahn P ( 1972 ) Untersuchungen zur Entwicklung von Ganz- und Teilimplantaten der Flu?gelimaginalscheibe von Ephestia ku?hniella Z . Dev Genes Evol 170 : 48 - 82 . http://dx.doi.org/10.1007/ BF00575521 42. Dewes E ( 1973 ) Regeneration in transplanted halves of male genital disks and its influence upon duration of development in Ephestia ku?hniella Z . Dev Genes Evol 172 : 349 - 354 . http://dx.doi.org/10.1007/ BF00577885 43. Dewes E ( 1975 ) Entwicklungsleistungen implantierter ganzer und halbierter ma?nnlicher Genitalimaginalscheiben von Ephestia kuehniella Z. und Entwicklungsdauer der Wirtstiere . Dev Genes Evol 178 : 167 - 183 . http://dx.doi.org/10.1007/BF00848395 44. Worley MI , Setiawan L , Hariharan IK ( 2012 ) Regeneration and transdetermination in Drosophila imaginal discs . Annu Rev Genet 46 : 289 - 310 . http://dx.doi.org/10.1146/annurev-genet- 110711 -155637 PMID: 22934642 45. Poodry CA , Woods DF ( 1990 ) Control of the developmental timer for Drosophila pupariation . Dev Genes Evol 199 : 219 - 227 . http://dx.doi.org/10.1007/BF01682081 46. Garelli A , Gontijo AM , Miguela V , Caparros E , Dominguez M ( 2012 ) Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation . Science 336 : 579 - 582 . http://dx.doi.org/10. 1126/science.1216735 PMID: 22556250 47. Colombani J , Andersen DS , Leopold P ( 2012 ) Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing . Science 336 : 582 - 585 . http://dx.doi.org/10.1126/science.1216689 PMID: 22556251 48. Waddington CH , Robertson E ( 1969 ) Determination, activation and actinomycin D insensitivity in the optic imaginal disk of Drosophila . Nature 221 : 933 - 935 . http://dx.doi.org/10.1038/221933a0 PMID: 5765504 49. Shingleton AW , Das J , Vinicius L , Stern DL ( 2005 ) The temporal requirements for insulin signaling during development in Drosophila . PLoS Biol 3 : e289 . http://dx.doi.org/10.1371/journal.pbio. 0030289 PMID: 16086608 50. Bo?hni R , Riesgo-Escovar J , Oldham S , Brogiolo W , Stocker H , Andruss BF , et al. ( 1999 ) Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4 . Cell 97 : 865 - 875 . http://dx.doi.org/10.1016/S0092- 8674 ( 00 ) 80799 - 0 PMID: 10399915 51. Kramer JM , Davidge JT , Lockyer JM , Staveley BE ( 2003 ) Expression of Drosophila FOXO regulates growth and can phenocopy starvation . BMC Dev Biol 3 : 5 . http://dx.doi. org/10.1186/1471-213X-3-5 PMID: 12844367 52. Sehnal F , Bryant PJ ( 1993 ) Delayed pupariation in Drosophila imaginal disc overgrowth mutants is associated with reduced ecdysteroid titer . J Insect Physiol 39 : 1051 - 1059 . http://dx.doi.org/10.1016/ 0022 - 1910 ( 93 ) 90129 -F 53. Gateff E ( 1978 ) Malignant neoplasms of genetic origin in Drosophila melanogaster . Science 200 : 1448 - 1459 . http://dx.doi.org/10.1126/science.96525 PMID: 96525 54. Hadorn E ( 1937 ) An Accelerating Effect of Normal ?Ring-Glands? on Puparium-Formation in Lethal Larvae of Drosophila Melanogaster . Proc Natl Acad Sci USA 23 : 478 - 484 . http://dx.doi. org/10.1073/pnas. 23.9.478 PMID: 16577798 55. Hackney JF , Zolali-Meybodi O , Cherbas P ( 2012 ) Tissue damage disrupts developmental progression and ecdysteroid biosynthesis in Drosophila . PLoS One 7 : e49105 . http://dx.doi.org/10.1371/journal. pone. 0049105 PMID: 23166607 56. Simpson P , Schneiderman HA ( 1975 ) Isolation of temperature sensitive mutations blocking clone development in Drosophila melanogaster, and the effects of a temperature sensitive cell lethal mutation on pattern formation in imaginal discs . Wilhelm Roux's Arch Dev Biol 178 : 247 - 275 . http://dx.doi.org/10. 1007/BF00848432 PMID: 28304775 57. Bourgin RC , Krumins R , Quastler H ( 1956 ) Radiation-Induced Delay of Pupation in Drosophila . Radiat Res 5 : 657 - 673 . http://dx.doi.org/10.2307/3570585 PMID: 13379619 58. Halme A , Cheng M , Hariharan IK ( 2010 ) Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila . Curr Biol 20 : 458 - 463 . http://dx.doi.org/10.1016/j.cub. 2010 . 01 .038 PMID: 20189388 59. Kiss I , Molnar I ( 1980 ) Metamorphic changes of wild type and mutant Drosophila tissues induced by 20- hydroxy ecdysone in vitro . J Insect Physiol 26 : 391 - 401 . http://dx.doi.org/10.1016/ 0022 - 1910 ( 80 ) 90010 - 4 60. Yamanaka N , Rewitz KF , O'Connor MB ( 2013 ) Ecdysone Control of Developmental Transitions: Lessons from Drosophila Research . Annu Rev Entomol 58 : 497 - 516 . http://dx.doi.org/10.1146/annurevento-120811 -153608 PMID: 23072462 61. Riddiford LM , Truman JW ( 1993 ) Hormone receptors and the regulation of insect metamorphosis . Amer Zool 3 : 340 - 347 . https://doi.org/10.1093/icb/33.3.340 PMID: 8167571 62. Simpson P , Berreur P , Berreur-Bonnenfant J ( 1980 ) The initiation of pupariation in Drosophila: dependence on growth of the imaginal discs . J Embryol Exp Morphol 57 : 155 - 165 . PMID: 7430927 63. Andres AJ , Cherbas P ( 1992 ) Tissue-specific ecdysone responses: regulation of the Drosophila genes Eip28/29 and Eip40 during larval development . Development 116 : 865 - 876 . PMID: 1295740 64. Johnson DG , Walker CL ( 1999 ) Cyclins and cell cycle checkpoints . Annu Rev Pharmacol Toxicol 39 : 295 - 312 . http://dx.doi.org/10.1146/annurev. pharmtox.39.1.295 PMID: 10331086 65. Atli E , Unlu? H ( 2006 ) The effects of microwave frequency electromagnetic fields on the development of Drosophila melanogaster . Int J Radiat Biol 82 : 435 - 441 . http://dx.doi.org/10.1080/ 09553000600798849 PMID: 16846978 66. Pohley H ( 1965 ) Regeneration and the moulting cycle in Ephestia kuhniella . In: Kiortis V , Trampusch H , eds. Regeneration in Animals. Amsterdam: North Holland Pub Co 324-330. 67. Brindley H ( 1897 ) On the regeneration of the legs in the Blattidae . Zool Soc Proc 907 - 916 . http://dx.doi. org/10.1111/j.1096- 3642 . 1898 .tb01392.x 68. French V ( 1976 ) Leg regeneration in the cockroach, Blattella germanica . Dev Genes Evol 179 : 57 - 76 . http://dx.doi.org/10.1007/BF00857640 PMID: 939940 69. Bullie?re D , Bullie?re F ( 1985 ) Regeneration . Comprehensive insect physiology, biochemistry and pharmacology , pp. 371 - 424 In Kerkut GA , Gilbert LI . [eds.], Pergamon Press, Oxford, UK. 70. Villee CA ( 1946 ) Some effects of x-rays on development in Drosophila . J Exp Zool 101 : 261 - 280 . http://dx.doi.org/10.1002/jez.1401010206 PMID: 21022220 71. Marks EP , Leopold RA ( 1970 ) Coackroach leg regeneration: Effects of ecdysterone in vitro . Science 167 : 61 - 62 . http://dx.doi. org/10.1126/science.167.3914.61 PMID: 5409478 72. O 'farrell AF , Stock A , Morgan J ( 1956 ) Regeneration and the moulting cycle in Blattella germanica L. IV. Single and repeated regeneration and metamorphosis . Aust J Biol Sci 6 : 406 - 422 . https://doi.org/10. 1071/BI9560406 73. Johnson SA , Jakob EM ( 1999 ) Leg autotomy in a spider hasminimal costs in competitive ability and development . Anim Behav 57 : 957 - 965 . https://doi.org/10.1006/anbe. 1998 .1058 PMID: 10202103 74. Emmel VE ( 1907 ) Regeneration and the question of ?symmetry in https://doi .org/10.1126/science.26. 655.83 PMID: 17743207 big claws of the lobster? . Science 26 : 83 - 87 . https://doi.org/10.1126/science. 26.655.83 75. Frasnelli EG , Vallortigara G , Rogers LJ ( 2012 ) Left-right asymmetries of behaviour and nervous system in invetebrates . Neurosci Biobehav R 36 : 1273 - 1291 . https://doi.org/10.1016/j.neubiorev. 2012 . 02 .006 PMID: 22353424 76. Shearn A , Rice T , Garen A , Gehring W ( 1971 ) Imaginal disc abnormalities in lethal mutants of Drosophila . Proc Natl Acad Sci USA 68 : 2594 - 2598 . http://dx.doi.org/10.1073/pnas.68.10.2594 PMID: 5002822 77. Szabad J , Bryant PJ ( 1982 ) The mode of action of ?discless? mutations in Drosophila melanogaster . Dev Biol 93 : 240 - 256 . http://dx.doi.org/10.1016/ 0012 - 1606 ( 82 ) 90256 - 1 PMID: 6813163 78. Stevens ME , Bryant PJ ( 1986 ) Temperature-dependent expression of the apterous phenotype in Drosophila melanogaster . Genetics 112 : 217 - 228 . PMID: 3079719 79. Shi W , Stampas A , Zapata C , Baker NE ( 2003 ) The pineapple eye gene is required for survival of Drosophila imaginal disc cells . Genetics 165 : 1869 - 1879 . PMID: 14704172


This is a preview of a remote PDF: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0210615&type=printable

Pengxiang Wu, Fengming Wu, Shuo Yan, Chang Liu, Zhongjian Shen, Xiaofei Xiong, Zhen Li, Qingwen Zhang, Xiaoxia Liu. Developmental cost of leg-regenerated Coccinella septempunctata (Coleoptera: Coccinellidae), PLOS ONE, 2019, DOI: 10.1371/journal.pone.0210615