Prolonged milk provisioning and extended maternal care in the milking spider <i>Toxeus magnus</i>: biological implications and questions unresolved

Bing Dong; Rui-Chang Quan; Zhan-Qi Chen

doi:10.24272/j.issn.2095-8137.2019.041

Volume 40 Issue 4

Jul. 2019

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Bing Dong, Rui-Chang Quan, Zhan-Qi Chen. Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved. Zoological Research, 2019, 40(4): 241-243. doi: 10.24272/j.issn.2095-8137.2019.041

Citation:

Bing Dong, Rui-Chang Quan, Zhan-Qi Chen. Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved. Zoological Research, 2019, 40(4): 241-243. doi: 10.24272/j.issn.2095-8137.2019.041

Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved

doi: 10.24272/j.issn.2095-8137.2019.041

1.
CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Xishuangbanna Yunnan 666303, China
2.
Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Xishuangbanna Yunnan 666303, China
3.
University of Chinese Academy of Sciences, Beijing 100049, China

Funds: This study was supported by the National Natural Science Foundation of China (30800121)

More Information

Corresponding author: Rui-Chang Quan,Zhan-Qi Chen
Received Date: 2019-05-13
Publish Date: 2019-07-18

Abstract

Prolonged milk provisioning and extended parental care for nutritionally independent offspring, previously considered to only co-occur in long-lived mammals (Clutton-Brock, 1991; Royle et al., 2012), were recently reported in the reproduction of the milking spider, Toxeus magnus (Chen et al. 2018). Newly hatched T. magnus spiderlings require 53 days to develop to maturity, with an average adult body length of 6.6 mm. The mother provides milk droplets to her newly hatched spiderlings until they develop into subadults (~38 days old), during which their body lengths increase from 0.9 mm at birth to 5.3 mm at weaning. Although spiderlings can forage for themselves at around 20 days old, they remain in the breeding nest for weeks after maturity.
- Toxeus magnus,
- Spider milk,
- Parental care,
- Food provisioning

References

[1]

null	Benoit JB , Attardo GM , Baumann AA , Michalkova V , Aksoy S . 2015. Adenotrophic viviparity in tsetse flies: potential for population control and as an insect model for lactation. Annual Review of Entomology, 60(1): 351–371.
null	Bilinski SM , Jaglarz MK , Halajian A , Tworzydlo W . 2018. Unusual morphological adaptations and processes associated with viviparity in an epizoic dermapteran. PLoS One, 13(4): e0195647.
null	Brown C , Laland K . 2001. Social learning and life skills training for hatchery reared fish. Journal of Fish Biology, 59(3): 471–493.
null	Chen ZQ , Corlett RT , Jiao XG , Liu SJ , Charles-Dominique T , Zhang SC , Li H , Lai R , Long CB , Quan RC . 2018. Prolonged milk provisioning in a jumping spider. Science, 362(6418): 1052–1055.
null	Clutton-Brock TH . 1991. The Evolution of Parental Care. Princeton, NJ: Princeton University Press.
null	Curio E . 1993. Proximate and developmental aspects of antipredator behavior. Advances in the Study of Behavior, 22: 135–238.
null	Davies NB , Welbergen JA . 2009. Social transmission of a host defense against cuckoo parasitism. Science, 324(5932): 1318–1320.
null	Demmelmair H , Prell C , Timby N , L?nnerdal B . 2017. Benefits of lactoferrin, osteopontin and milk fat globule membranes for infants. Nutrients, 9(8): 817.
null	Gélin U , Wilson ME , Coulson G , Festa-Bianchet M . 2015. Experimental manipulation of female reproduction demonstrates its fitness costs in kangaroos. Journal of Animal Ecology, 84(1): 239–248.
null	George LA , Uthlaut AB , Long NM , Zhang L , Ma Y , Smith DT , Nathanielsz PW , Ford SP . 2010. Different levels of overnutrition and weight gain during pregnancy have differential effects on fetal growth and organ development. Reproductive Biology and Endocrinology, 8(1): 75.
null	Gittleman JL , Thompson SD . 1988. Energy allocation in mammalian reproduction. American Zoologist, 28(3): 863–875.
null	Glazier DS . 1985. Relationship between metabolic rate and energy expenditure for lactation in Peromyscus. Comparative Biochemistry and Physiology Part A: Physiology, 80(4): 587–590.
null	Hayssen V . 1993. Empirical and theoretical constraints on the evolution of lactation. Journal of Dairy Science, 76(10): 3213–3233.
null	Hoppitt WJE , Brown GR , Kendal R , Rendell L , Thornton A , Webster MM , Laland KN . 2008. Lessons from animal teaching. Trends in Ecology & Evolution, 23(9): 486–493.
null	McCGraham N . 1964. Energy exchanges of pregnant and lactating ewes. Australian Journal of Agricultural Research, 15(1): 127–141.
null	McClure PA . 1987. The energetics of reproduction and life histories of cricetine rodents. Symposium of the Zoological Society of London, 57: 241–258.
null	Millar JS . 1978. Energetics of reproduction in Peromyscus leucopus: the cost of lactation. Ecology, 59(5): 1055–1061.
null	Oftedal OT . 2002. The origin of lactation as a water source for parchment-shelled eggs. Journal of Mammary Gland Biology and Neoplasia, 7(3): 253–266.
null	Ostrovsky AN, Lidgard S , Gordon DP , Schwaha T , Genikhovich G , Ereskovsky AV . 2016. Matrotrophy and placentation in invertebrates: a new paradigm. Biological Reviews, 91(3): 673–711.
null	Page KC , Malik RE , Ripple JA , Anday EK . 2009. Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 297(4): R1049–R1057.
null	Royle NJ , Smiseth PT , K?lliker M . 2012. The Evolution of Parental Care. Oxford, UK: Oxford University Press.
null	Surbeck M , Mundry R , Hohmann G . 2011. Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proceedings of the Royal Society B-Biological Sciences, 278(1705): 590–598.
null	Taylor PD , McConnell J , Khan IY , Holemans K , Lawrence KM , Asare-Anane H , Persaud SJ , Jones PM , Petrie L , Hanson MA , Poston L . 2005. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 288(1): R134–R139.
null	Vorbach C , Capecchi MR , Penninger JM . 2006. Evolution of the mammary gland from the innate immune system?. Bioessays, 28(6): 606–616.
null	Ward RE , German JB . 2004. Understanding milk’s bioactive components: a goal for the genomics toolbox. The Journal of Nutrition, 134(4): 962S–967S.
null	Wong JW , Meunier J , K?elliker M . 2013. The evolution of parental care in insects: the roles of ecology, life history and the social environment. Ecological Entomology, 38(2): 123–137.

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通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142

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Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved

1. CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Xishuangbanna Yunnan 666303, China

2. Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Xishuangbanna Yunnan 666303, China

3. University of Chinese Academy of Sciences, Beijing 100049, China

Funds: This study was supported by the National Natural Science Foundation of China (30800121)

Corresponding author: Rui-Chang Quan,Zhan-Qi Chen

Received Date: 2019-05-13

Publish Date: 2019-07-18

Key words:

Abstract: Prolonged milk provisioning and extended parental care for nutritionally independent offspring, previously considered to only co-occur in long-lived mammals (Clutton-Brock, 1991; Royle et al., 2012), were recently reported in the reproduction of the milking spider, Toxeus magnus (Chen et al. 2018). Newly hatched T. magnus spiderlings require 53 days to develop to maturity, with an average adult body length of 6.6 mm. The mother provides milk droplets to her newly hatched spiderlings until they develop into subadults (~38 days old), during which their body lengths increase from 0.9 mm at birth to 5.3 mm at weaning. Although spiderlings can forage for themselves at around 20 days old, they remain in the breeding nest for weeks after maturity.

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Reference (1)

[1]

null	Benoit JB , Attardo GM , Baumann AA , Michalkova V , Aksoy S . 2015. Adenotrophic viviparity in tsetse flies: potential for population control and as an insect model for lactation. Annual Review of Entomology, 60(1): 351–371.
null	Bilinski SM , Jaglarz MK , Halajian A , Tworzydlo W . 2018. Unusual morphological adaptations and processes associated with viviparity in an epizoic dermapteran. PLoS One, 13(4): e0195647.
null	Brown C , Laland K . 2001. Social learning and life skills training for hatchery reared fish. Journal of Fish Biology, 59(3): 471–493.
null	Chen ZQ , Corlett RT , Jiao XG , Liu SJ , Charles-Dominique T , Zhang SC , Li H , Lai R , Long CB , Quan RC . 2018. Prolonged milk provisioning in a jumping spider. Science, 362(6418): 1052–1055.
null	Clutton-Brock TH . 1991. The Evolution of Parental Care. Princeton, NJ: Princeton University Press.
null	Curio E . 1993. Proximate and developmental aspects of antipredator behavior. Advances in the Study of Behavior, 22: 135–238.
null	Davies NB , Welbergen JA . 2009. Social transmission of a host defense against cuckoo parasitism. Science, 324(5932): 1318–1320.
null	Demmelmair H , Prell C , Timby N , L?nnerdal B . 2017. Benefits of lactoferrin, osteopontin and milk fat globule membranes for infants. Nutrients, 9(8): 817.
null	Gélin U , Wilson ME , Coulson G , Festa-Bianchet M . 2015. Experimental manipulation of female reproduction demonstrates its fitness costs in kangaroos. Journal of Animal Ecology, 84(1): 239–248.
null	George LA , Uthlaut AB , Long NM , Zhang L , Ma Y , Smith DT , Nathanielsz PW , Ford SP . 2010. Different levels of overnutrition and weight gain during pregnancy have differential effects on fetal growth and organ development. Reproductive Biology and Endocrinology, 8(1): 75.
null	Gittleman JL , Thompson SD . 1988. Energy allocation in mammalian reproduction. American Zoologist, 28(3): 863–875.
null	Glazier DS . 1985. Relationship between metabolic rate and energy expenditure for lactation in Peromyscus. Comparative Biochemistry and Physiology Part A: Physiology, 80(4): 587–590.
null	Hayssen V . 1993. Empirical and theoretical constraints on the evolution of lactation. Journal of Dairy Science, 76(10): 3213–3233.
null	Hoppitt WJE , Brown GR , Kendal R , Rendell L , Thornton A , Webster MM , Laland KN . 2008. Lessons from animal teaching. Trends in Ecology & Evolution, 23(9): 486–493.
null	McCGraham N . 1964. Energy exchanges of pregnant and lactating ewes. Australian Journal of Agricultural Research, 15(1): 127–141.
null	McClure PA . 1987. The energetics of reproduction and life histories of cricetine rodents. Symposium of the Zoological Society of London, 57: 241–258.
null	Millar JS . 1978. Energetics of reproduction in Peromyscus leucopus: the cost of lactation. Ecology, 59(5): 1055–1061.
null	Oftedal OT . 2002. The origin of lactation as a water source for parchment-shelled eggs. Journal of Mammary Gland Biology and Neoplasia, 7(3): 253–266.
null	Ostrovsky AN, Lidgard S , Gordon DP , Schwaha T , Genikhovich G , Ereskovsky AV . 2016. Matrotrophy and placentation in invertebrates: a new paradigm. Biological Reviews, 91(3): 673–711.
null	Page KC , Malik RE , Ripple JA , Anday EK . 2009. Maternal and postweaning diet interaction alters hypothalamic gene expression and modulates response to a high-fat diet in male offspring. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 297(4): R1049–R1057.
null	Royle NJ , Smiseth PT , K?lliker M . 2012. The Evolution of Parental Care. Oxford, UK: Oxford University Press.
null	Surbeck M , Mundry R , Hohmann G . 2011. Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proceedings of the Royal Society B-Biological Sciences, 278(1705): 590–598.
null	Taylor PD , McConnell J , Khan IY , Holemans K , Lawrence KM , Asare-Anane H , Persaud SJ , Jones PM , Petrie L , Hanson MA , Poston L . 2005. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 288(1): R134–R139.
null	Vorbach C , Capecchi MR , Penninger JM . 2006. Evolution of the mammary gland from the innate immune system?. Bioessays, 28(6): 606–616.
null	Ward RE , German JB . 2004. Understanding milk’s bioactive components: a goal for the genomics toolbox. The Journal of Nutrition, 134(4): 962S–967S.
null	Wong JW , Meunier J , K?elliker M . 2013. The evolution of parental care in insects: the roles of ecology, life history and the social environment. Ecological Entomology, 38(2): 123–137.

Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved

doi: 10.24272/j.issn.2095-8137.2019.041

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Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved

doi: 10.24272/j.issn.2095-8137.2019.041

Corresponding author: Rui-Chang Quan,Zhan-Qi Chen

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Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved

doi: 10.24272/j.issn.2095-8137.2019.041

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References

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通讯作者: 陈斌, bchen63@163.com

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Prolonged milk provisioning and extended maternal care in the milking spider Toxeus magnus: biological implications and questions unresolved

doi: 10.24272/j.issn.2095-8137.2019.041

Corresponding author: Rui-Chang Quan,Zhan-Qi Chen

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