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Effects of dietary restriction on lifespan, growth, and reproduction of the clam shrimp Eulimnadia texana

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Abstract

Diet has been linked to lifespan in a broad range of animals. In particular, pronounced caloric restriction has been associated with increased longevity. Herein, the relationship of feeding environment and longevity is examined experimentally using Spinicaudatan crustaceans (“clam shrimp”) from the geographically widespread genus Eulimnadia. Two projects examine the effects of food differences on longevity, one comparing food environment early vs later in life and one comparing the effects of dietary restriction on longevity, growth, and reproduction. In the former, dietary restriction increased longevity, but only when diets were reduced later in life. A closer examination of the effects of dietary restriction in the second experiment did not find the expected trade-off of increased longevity and reduced reproductive output in the lowest-food treatment, but instead found an overall increase in both longevity and egg production on the low compared to the high food diet. Finally, a detailed analysis of the relationship of size (carapace length) with egg production was presented. This relationship could serve to obtain a rough estimate of reproductive output potential of fossil clam shrimps, of which typically only the carapace size can be assessed.

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Fig. 1
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Data from Weeks (2004), Weeks & Bernhardt (2004) and Weeks et al. (2014a)

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References

  • Astrop, T. I., V. Sahni, T. A. Blackledge & A. Y. Stark, 2015. Mechanical properties of the chitin-calcium-phosphate “clam shrimp” carapace (Branchiopoda: Spinicaudata): implications for taphonomy and fossilization. Journal of Crustacean Biology 35: 123–131.

    Article  Google Scholar 

  • Balasubramanian, P., P. R. Howell & R. M. Anderson, 2017. Aging and caloric restriction research: a biological perspective with translational potential. Ebiomedicine 21: 37–44.

    Article  PubMed  PubMed Central  Google Scholar 

  • Belk, D., 1972. The biology and ecology of Eulimnadia antlei Mackin (Conchostraca). Southwestern Naturalist 16: 297–305.

    Article  Google Scholar 

  • Brantner, J. S., D. W. Ott, R. J. Duff, J. I. Orridge, J. R. Waldman & S. C. Weeks, 2013a. Evidence of selfing hermaphroditism in the clam shrimp Cyzicus gynecia (Branchiopoda: Spinicaudata). Journal of Crustacean Biology 33: 184–190.

    Article  Google Scholar 

  • Brantner, J. S., D. W. Ott, R. J. Duff, L. O. Sanoamuang, G. P. Simhachalam, K. K. S. Babu & S. C. Weeks, 2013b. Androdioecy and hermaphroditism in five species of clam shrimps (Crustacea: Branchiopoda: Spinicaudata) from India and Thailand. Invertebrate Biology 132: 27–37.

    Article  Google Scholar 

  • Calabrese, A., C. McCulloch, B. Knott & S. C. Weeks, 2016. Environmental characteristics of ephemeral rock pools explain local abundances of the clam shrimp, Paralimnadia badia (Branchiopoda: Spinicaudata: Limnadiidae). Journal of the Royal Society of Western Australia 99: 9–15.

    Google Scholar 

  • Chen, P.-J. & J. D. Hudson, 1991. The conchostracan fauna of the Great Estuarine Group, Middle Jurassic, Scotland. Palaeontology 34: 515–545.

    Google Scholar 

  • Chen, P.-J. & Y. B. Shen, 1985. Fossil Conchostraca. Science Press, Beijing.

    Google Scholar 

  • Clutton-Brock, T. & P. Langley, 1997. Persistent courtship reduces male and female longevity in captive tsetse flies Glossina morsitans morsitans Westwood (Diptera: Glossinidae). Behavioral Ecology 8: 392–395.

    Article  Google Scholar 

  • Comfort, A., 1979. The Biology of Senescence, 3rd ed. Churchill Livingston, Edinburgh.

    Google Scholar 

  • Currie, J. J. & D. C. Schneider, 2011. Spatial scaling from latitudinal gradients: size-specific fecundity in the American lobster Homarus americanus. Marine Ecology Progress Series 439: 193–201.

    Article  Google Scholar 

  • Dumont, H. J. & S. V. Negrea, 2002. Introduction to the class Branchiopoda. Backhuys, Leiden.

    Google Scholar 

  • Durga-Prasad, M. K. & G. Simhachalam, 2004. Eulimnadia indocylindrova n. sp. (Branchiopoda: Spinicaudata) from South India with a review of the genus Eulimnadia in Indomalayan region. Proceedings of the International Conference The Great Himalayas: Climate, Health, Ecology, Management, and Conservation.

  • Eder, E., S. Richter, R. Gottwald & W. Hodl, 2000. First record of Limnadia lenticularis males in Europe (Branchiopoda: Conchostraca). Journal of Crustacean Biology 20: 657–662.

    Article  Google Scholar 

  • Gallego, O. F. & C. Breitkreuz, 1994. Paleozoic Chonchostracans (Crustaceae-Conchostraca) from Antofagasta Region, Northern Chile. Revista Geologica De Chile 21: 31–53.

    Google Scholar 

  • Gems, D. & D. L. Riddle, 2000. Defining wild-type life span in Caenorhabditis elegans. Journals of Gerontology Series a-Biological Sciences and Medical Sciences 55: B215–B219.

    Article  CAS  Google Scholar 

  • Geyer, G. & K. P. Kelber, 2018. Spinicaudata (“Conchostraca,” Crustacea) from the Middle Keuper (Upper Triassic) of the southern Germanic Basin, with a review of Carnian-Norian taxa and suggested biozones. Palz 92: 1–34.

    Article  Google Scholar 

  • Green, B. S., C. Gardner & R. B. Kennedy, 2009. Generalised linear modelling of fecundity at length in southern rock lobsters, Jasus edwardsii. Marine Biology 156: 1941–1947.

    Article  Google Scholar 

  • Gueriau, P., N. Rabet & E. D. T. Hat, 2018. The Strud crustacean fauna (Late Devonian, Belgium): updated review and palaeoecology of an early continental ecosystem. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 107: 79–90.

    Article  Google Scholar 

  • Harper, J. L., 1977. The Population Biology of Plants. Academic Press, London/New York.

    Google Scholar 

  • Hethke, M., F. T. Fursich, J. D. Morton & B. Y. Jiang, 2018. Analysis of morphological variability in the clam shrimp Eosestheria middendorfii (Crustacea, Spinicaudata) from the lower Cretaceous of China, and its implications for Spinicaudatan taxonomy. Papers in Palaeontology 4: 21–53.

    Article  Google Scholar 

  • Hethke, M., F. T. Fursich, B. Y. Jiang, B. Wang, P. Chellouche & S. C. Weeks, 2019. Ecological stasis in Spinicaudata (Crustacea, Branchiopoda)? Early Cretaceous clam shrimp of the Yixian Formation of north-east China occupied a broader realized ecological niche than extant members of the group. Palaeontology 62: 483–513.

    Article  Google Scholar 

  • Huang, W. P. & L. S. Chou, 2015. Temperature effect on development and reproduction of the androdioecious clam shrimp, Eulimnadia braueriana (Branchiopoda: Spinicaudata). Journal of Crustacean Biology 35: 330–338.

    Article  Google Scholar 

  • Huang, W. P. & L. S. Chou, 2017. Temperature effects on life history traits of two sympatric branchiopods from an ephemeral wetland. PLoS ONE 12: 18.

    Google Scholar 

  • Johnson, T. E. & E. W. Hutchinson, 1993. Absence of strong heterosis for life-span and other life-history traits in Caenorhabditis elegans. Genetics 134: 465–474.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kirkwood, T. B. L. & D. P. Shanley, 2005. Food restriction, evolution and ageing. Mechanisms of Ageing and Development 126: 1011–1016.

    Article  PubMed  Google Scholar 

  • Knoll, L. & N. Zucker, 1995. Selfing versus outcrossing in the androdioecious clam shrimp, Eulimnadia texana (Crustacea, Conchostraca). Hydrobiologia 298: 83–86.

    Article  Google Scholar 

  • Kobayashi, T., 1954. Fossil Estherians and allied fossils. Journal of the Faculty of Science, University of Tokyo, section 2(9): 1–192.

    Google Scholar 

  • Lemaitre, J. F., V. Berger, C. Bonenfant, M. Douhard, M. Gamelon, F. Plard & J. M. Gaillard, 2015. Early-late life trade-offs and the evolution of ageing in the wild. Proceedings of the Royal Society B-Biological Sciences 282: 10.

    Article  Google Scholar 

  • Li, G., 2017. Morphological restudy of the type species of Xibeiestheria (Spinicaudata) from the lower Aptian, northwestern China. Cretaceous Research 80: 31–37.

    Article  Google Scholar 

  • Mackin, J. G., 1940. A new species of conchostracan phyllopod, Eulimnadia antlei, from Oklahoma. American Midland Naturalist 23: 219–221.

    Article  Google Scholar 

  • Maeda-Martinez, A. M., 1991. Distribution of Species of Anostraca, Notostraca, Spinicaudata, and Laevicaudata in Mexico. Hydrobiologia 212: 209–219.

    Article  Google Scholar 

  • Martin, J. W., 1989. Eulimnadia belki, a new clam shrimp from Cozumel, Mexico (Conchostraca, Limnadiidae), with a review of central and South American species of the genus Eulimnadia. Journal of Crustacean Biology 9: 104–114.

    Article  Google Scholar 

  • Martin, J. W. & D. Belk, 1989. Eulimnadia ovilunata and Eulimnadia ovisimilis, New species of clam shrimps (Crustacea, Branchiopoda, Spinicaudata) from South America. Proceedings of the Biological Society of Washington 102: 894–900.

    Google Scholar 

  • Masoro, E. J., 1988. Food restriction in rodents—an evaluation of its role in the study of aging. Journals of Gerontology 43: B59–B64.

    Article  CAS  PubMed  Google Scholar 

  • Mattox, N. T., 1939. Description of two new species of the genus Eulimnadia and notes on the other Phyllopoda of Illinois. American Midland Naturalist 22: 642–653.

    Article  Google Scholar 

  • McCulloch, D. & D. Gems, 2003. Evolution of male longevity bias in nematodes. Aging Cell 2: 165–173.

    Article  CAS  PubMed  Google Scholar 

  • Monferran, M. D., O. F. Gallego & N. G. Cabaleri, 2013. The first record of the family Fushunograptidae (‘Conchostraca’, Spinicaudata) from the Canadon Asfalto formation (upper Jurassic), Patagonia, Argentina. Ameghiniana 50: 447–459.

    Article  Google Scholar 

  • Morton, J. D., D. I. Whiteside, M. Hethke & M. J. Benton, 2017. Biostratigraphy and geometric morphometrics of conchostracans (Crustacea, Branchiopoda) from the Late Triassic fissure deposits of Cromhall Quarry, UK. Palaeontology 60: 349–374.

    Article  Google Scholar 

  • Olesen, J. & M. J. Grygier, 2003. Larval development of Japanese ‘conchostracans’: part 1, larval development of Eulimnadia braueriana (Crustacea, Branchiopoda, Spinicaudata, Limnadiidae) compared to that of other limnadiids. Acta Zoologica 84: 41–61.

    Article  Google Scholar 

  • Orr, P. J. & D. E. G. Briggs, 1999. Exceptionally preserved conchostracans and other crustaceans from the Upper Carboniferous of Ireland. Special Papers in Palaeontology Series 62: 5–68.

    Google Scholar 

  • Orr, P. J., D. E. G. Briggs & S. L. Kearns, 2008. Taphonomy of exceptionally preserved crustaceans from the Upper Carboniferous of southeastern Ireland. Palaios 23: 298–312.

    Article  Google Scholar 

  • Padhye, S. M. & E. A. Lazo-Wasem, 2018. An updated and detailed taxonomical account of the large Branchiopoda (Crustacea: Branchiopoda: Anostraca, Notostraca, Spinicaudata) from the Yale North India Expedition deposited in the Yale Peabody Natural History Museum. Zootaxa 4394: 207–218.

    Article  PubMed  Google Scholar 

  • Pereira, G. & J. V. Garcia, 2001. A review of the clam shrimp family Limnadiidae (Branchiopoda, Conchostraca) from Venezuela, with the description of a new species. Journal of Crustacean Biology 21: 640–652.

    Article  Google Scholar 

  • Perez-Bote, J. L., J. P. G. Piriz & A. G. Solis, 2014. Biological traits of Cyzicus grubei (Crustacea, Spinicaudata, Cyzicidae) in south-western Iberian Peninsula. Limnetica 33: 227–235.

    Google Scholar 

  • Phelan, J. P. & M. R. Rose, 2005. Why dietary restriction substantially increases longevity in animal models but won’t in humans. Ageing Research Reviews 4: 339–350.

    Article  CAS  PubMed  Google Scholar 

  • Reed, S. K., R. J. Duff & S. C. Weeks, 2015. A systematic study of the genus Eulimnadia. Journal of Crustacean Biology 35: 379–391.

    Article  Google Scholar 

  • Rogers, D. C., N. Rabet & S. C. Weeks, 2012. Revision of the extant genera of Limnadiidae (Branchiopoda: Spinicaudata). Journal of Crustacean Biology 32: 827–842.

    Article  Google Scholar 

  • Rose, M. R., 1991. Evolutionary Biology of Aging. Oxford University Press, New York.

    Google Scholar 

  • Sassaman, C., 1989. Inbreeding and sex-ratio variation in female-biased populations of a clam shrimp, Eulimnadia texana. Bulletin of Marine Science 45: 425–432.

    Google Scholar 

  • Sassaman, C., 1995. Sex determination and evolution of unisexuality in the Conchostraca. Hydrobiologia 298: 45–65.

    Article  Google Scholar 

  • Sassaman, C. & S. C. Weeks, 1993. The genetic mechanism of sex determination in the conchostracan shrimp Eulimnadia texana. American Naturalist 141: 314–328.

    Article  CAS  PubMed  Google Scholar 

  • Schwentner, M., B. V. Timms, R. Bastrop & S. Richter, 2009. Phylogeny of Spinicaudata (Branchiopoda, Crustacea) based on three molecular markers—an Australian origin for Limnadopsis. Molecular Phylogenetics and Evolution 53: 716–725.

    Article  PubMed  Google Scholar 

  • Shen, Y. B., 1994. Jurassic Conchostracans from Carapace Nunatak, Southern Victoria Land, Antarctica. Antarctic Science 6: 105–113.

    Article  Google Scholar 

  • Smith, D. G., 1992. A redescription of types of the clam shrimp Eulimnadia agassizii (Spinicaudata, Limnadiidae). Transactions of the American Microscopical Society 111: 223–228.

    Article  Google Scholar 

  • Tasch, P., 1971. Invertebrate fossil record and continental drift. In Quam, L. O. (ed) Research in the Antarctic. Vol. Pub. No. 93. American Association for the Advancement of Science, Washington: 703–716.

  • Tasch, P., 1987. Fossil Conchostraca of the southern hermisphere and continental drift. Paleontology, biostratigraphy, and dispersal, Memoir 165 edn. Geological Society of America, Boulder.

  • Tasch, P. & B. L. Shaffer, 1964. Conchostracans: living and fossil from Chihuahua and Sonora, Mexico. Science 143: 806–807.

    Article  CAS  PubMed  Google Scholar 

  • Timms, B. V., 2016. A partial revision of the Australian Eulimnadia Packard, 1874 (Branchiopoda: Spinicaudata: Limnadiidae). Zootaxa 4066: 351–389.

    Article  PubMed  Google Scholar 

  • Timms, B. V. & S. Richter, 2009. The clam shrimp Eocyzicus (Branchiopoda: Spinicaudata: Cyzicidae) in Australia. Journal of Crustacean Biology 29: 245–253.

    Article  Google Scholar 

  • Tinti, F. & F. Scanabissi, 1996. Reproduction and genetic variation in clam shrimps (Crustacea, Branchiopoda, Conchostraca). Canadian Journal of Zoology-Revue Canadienne De Zoologie 74: 824–832.

    Article  CAS  Google Scholar 

  • Tippelt, L. & M. Schwentner, 2018. Taxonomic assessment of Australian Eocyzicus species (Crustacea: Branchiopoda: Spinicaudata). Zootaxa 4410: 401–452.

    Article  PubMed  Google Scholar 

  • Vannier, J., A. Thiery & P. R. Racheboeuf, 2003. Spinicaudatans and ostracods (Crustacea) from the Montceau Lagerstatte (Late Carboniferous, France): morphology and palaeoenvironmental significance. Palaeontology 46: 999–1030.

    Article  Google Scholar 

  • Vidrine, M. F., S. L. Sissom & R. E. McLaughlin, 1987. Eulimnadia texana Packard (Conchostraca, Limnadiidae) in rice fields in southwestern Louisiana. Southwestern Naturalist 32: 1–4.

    Article  Google Scholar 

  • Walossek, D., 1993. The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustaca. Fossils and Strata 32: 1–202.

    Google Scholar 

  • Webb, J. A. & G. D. Bell, 1979. A new species of Limnadia (Crustacea: Conchostraca) from the granite belt in southern Queensland and Northern New South Wales. Proceedings of the Linnean Society of New South Wales 103: 237–246.

    Google Scholar 

  • Weeks, S. C., 2004. Levels of inbreeding depression over seven generations of selfing in the androdioecious clam shrimp, Eulimnadia texana. Journal of Evolutionary Biology 17: 475–484.

    Article  CAS  PubMed  Google Scholar 

  • Weeks, S. C., 2012. The role of androdioecy and gynodioecy in mediating evolutionary transitions between dioecy and hermaphroditism in the Animalia. Evolution 66: 3670–3686.

    Article  PubMed  Google Scholar 

  • Weeks, S. C. & R. L. Bernhardt, 2004. Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: field estimates of inbreeding depression and relative male survival. Evolutionary Ecology Research 6: 227–242.

    Google Scholar 

  • Weeks, S. C. & N. Zucker, 1999. Rates of inbreeding in the androdioecious clam shrimp Eulimnadia texana. Canadian Journal of Zoology-Revue Canadienne De Zoologie 77: 1402–1408.

    Article  Google Scholar 

  • Weeks, S. C., V. Marcus & S. Alvarez, 1997. Notes on the life history of the clam shrimp, Eulimnadia texana. Hydrobiologia 359: 191–197.

    Article  Google Scholar 

  • Weeks, S. C., V. Marcus & B. R. Crosser, 1999. Inbreeding depression in a self-compatible, androdioecious crustacean, Eulimnadia texana. Evolution 53: 472–483.

    Article  PubMed  Google Scholar 

  • Weeks, S. C., B. R. Crosser, R. Bennett, M. Gray & N. Zucker, 2000. Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: estimates of inbreeding depression in two populations. Evolution 54: 878–887.

    Article  CAS  PubMed  Google Scholar 

  • Weeks, S. C., J. A. Hutchison & N. Zucker, 2001. Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: do hermaphrodites need males for complete fertilization? Evolutionary Ecology 15: 205–221.

    Article  Google Scholar 

  • Weeks, S. C., R. T. Posgai, M. Cesari & F. Scanabissi, 2005. Androdioecy inferred in the clam shrimp Eulimnadia agassizii (Spinicaudata: Limnadiidae). Journal of Crustacean Biology 25: 323–328.

    Article  Google Scholar 

  • Weeks, S. C., C. Benvenuto & S. K. Reed, 2006a. When males and hermaphrodites coexist: a review of androdioecy in animals. Integrative and Comparative Biology 46: 449–464.

    Article  PubMed  Google Scholar 

  • Weeks, S. C., S. K. Reed, M. Cesari & F. Scanabissi, 2006b. Production of intersexes and the evolution of androdioecy in the clam shrimp Eulimnadia texana (Crustacea, Branchiopoda, Spinicaudata). Invertebrate Reproduction & Development 49: 113–119.

    Article  Google Scholar 

  • Weeks, S. C., T. F. Sanderson, M. Zofkova & B. Knott, 2008. Breeding systems in the clam shrimp family Limnadiidae (Branchiopoda, Spinicaudata). Invertebrate Biology 127: 336–349.

    Article  Google Scholar 

  • Weeks, S. C., E. G. Chapman, D. C. Rogers, D. M. Senyo & W. R. Hoeh, 2009. Evolutionary transitions among dioecy, androdioecy and hermaphroditism in limnadiid clam shrimp (Branchiopoda: Spinicaudata). Journal of Evolutionary Biology 22: 1781–1799.

    Article  CAS  PubMed  Google Scholar 

  • Weeks, S. C., C. Benvenuto, T. F. Sanderson & R. J. Duff, 2010. Sex chromosome evolution in the clam shrimp, Eulimnadia texana. Journal of Evolutionary Biology 23: 1100–1106.

    Article  CAS  PubMed  Google Scholar 

  • Weeks, S. C., J. S. Brantner, T. I. Astrop, D. W. Ott & N. Rabet, 2014b. The evolution of hermaphroditism from dioecy in crustaceans: selfing hermaphroditism described in a fourth Spinicaudatan genus. Evolutionary Biology 41: 251–261.

    Article  Google Scholar 

  • Weeks, S. C., C. Benvenuto, S. K. Reed, R. J. Duff, Z. H. Duan & P. David, 2014a. A field test of a model for the stability of androdioecy in the freshwater shrimp, Eulimnadia texana. Journal of Evolutionary Biology 27: 2080–2095.

    Article  CAS  PubMed  Google Scholar 

  • Weindruch, R. & R. L. Walford, 1988. The retardation of aging and disease by dietary restriction. Charles C. Thomas, Springfield.

    Google Scholar 

  • Weindruch, R., R. L. Walford, S. Fligiel & D. Guthrie, 1986. The retardation of aging in mice by dietary restriction—longevity, cancer, immunity and lifetime energy-intake. Journal of Nutrition 116: 641–654.

    Article  CAS  PubMed  Google Scholar 

  • Zaffagnini, F., 1969. Rudimentary hermaphroditism and automictic parthenogenesis in Limnadia lenticularis (Phyllopoda, Conchostraca). Experientia 25: 650–651.

    Article  CAS  PubMed  Google Scholar 

  • Zinn, D. J. & R. W. Dexter, 1962. Reappearance of Eulimnadia agassizii with notes on its biology and life history. Science 137: 676–677.

    Article  CAS  PubMed  Google Scholar 

  • Zucker, N., M. Cunningham & H. P. Adams, 1997. Anatomical evidence for androdioecy in the clam shrimp Eulimnadia texana. Hydrobiologia 359: 171–175.

    Article  Google Scholar 

  • Zucker, N., B. Stafki & S. C. Weeks, 2001. Maintenance of androdioecy in the freshwater clam shrimp Eulimnadia texana: longevity of males relative to hermaphrodites. Canadian Journal of Zoology-Revue Canadienne De Zoologie 79: 393–401.

    Article  Google Scholar 

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Acknowledgements

I thank Susan Wiedman and Kasey Yates for rearing help in the lab. All data generated or analyzed during this study are included in this published article [and its supplementary information files].

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Weeks, S.C. Effects of dietary restriction on lifespan, growth, and reproduction of the clam shrimp Eulimnadia texana. Hydrobiologia 847, 3067–3076 (2020). https://doi.org/10.1007/s10750-020-04313-y

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