Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-19T00:44:45.838Z Has data issue: false hasContentIssue false
  • English
  • Français

Sexual dimorphism and sexual selection in cytheroidean ostracodes from the Late Cretaceous of the U.S. Coastal Plain

Published online by Cambridge University Press:  22 August 2017

Gene Hunt ,
M. João Fernandes Martins ,
T. Markham Puckett ,
Rowan Lockwood ,
John P. Swaddle ,
Christine M. S. Hall  and
James Stedman
Gene Hunt
Affiliation:
Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, U.S.A. E-mail: hunte@si.edu
M. João Fernandes Martins
Affiliation:
Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, U.S.A. E-mail: hunte@si.edu
T. Markham Puckett
Affiliation:
Department of Geography and Geology, University of Southern Mississippi, Hattiesburg, Mississippi 39406, U.S.A.
Rowan Lockwood
Affiliation:
Department of Geology, College of William and Mary, Williamsburg, Virginia 23187, U.S.A.
John P. Swaddle
Affiliation:
Department of Biology, College of William and Mary, Williamsburg, Virginia 23187, U.S.A.
Christine M. S. Hall
Affiliation:
Department of Earth Sciences, University of California, Riverside, Riverside, California 92521, U.S.A.
James Stedman
Affiliation:
Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, U.S.A. E-mail: hunte@si.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Sexual dimorphism is common in many extant animals, but it is difficult to demonstrate in fossil species. Working with material from the Late Cretaceous of the U.S. Coastal Plain, we herein analyze sexual dimorphism in ostracodes from the superfamily Cytheroidea, a group whose extant members have males that are relatively more elongate than females. We digitized outlines of more than 6000 individual ostracode valves or carapaces, extracted size (area) and shape (length-to-height ratio) information, and used finite mixture models to assess hypotheses of sexual dimorphism. Male and female clusters can be discerned in nearly all populations with sufficient data, resulting in estimates of size and shape dimorphism for 142 populations across 106 species; an additional nine samples are interpreted to consist only of females. Dimorphism patterns varied across taxa, especially for body size: males range from 30% larger to 20% smaller than females. Magnitudes of sexual dimorphism are generally stable within species across time and space; we can demonstrate substantial evolutionary changes in dimorphism in only one species, Haplocytheridea renfroensis. Several lines of evidence indicate that patterns of sexual dimorphism in these ostracodes reflect male investment in reproduction, suggesting that this study system has the potential to capture variation in sexual selection through the fossil record.

Type
Articles
Information
Paleobiology , Volume 43 , Issue 4 , November 2017 , pp. 620 - 641
Copyright
Copyright © 2017 The Paleontological Society. All rights reserved 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Abe, K. 1990. What the sex ratio tells us: a case from marine ostracods. Pp. 175–185. in R. Whatley, and C. Maybury, eds. Ostracoda and global events. Chapman and Hall, London.Google Scholar
Abe, K., and Vannier, J.. 1991. Mating behavior in the podocopid ostracode Bicornucythere bisanensis (Okubo, 1975): rotation of a female by a male with asymmetric 5th limbs. Journal of Crustacean Biology 11:250–260.Google Scholar
Abouheif, E., and Fairbairn, D. J.. 1997. A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. American Naturalist 149:540–562.CrossRefGoogle Scholar
Alexander, C. I. 1929. Ostracoda of the Cretaceous of north Texas. University of Texas Bulletin 2907:1–137.Google Scholar
Alexander, C. I. 1932. Sexual dimorphism in fossil Ostracoda. American Midland Naturalist 12:302–310.CrossRefGoogle Scholar
Alexander, C. I. 1933. Shell structure of the ostracode genus Cytheropteron, and fossil species from the Cretaceous of Texas. Journal of Paleontology 7:181–214.Google Scholar
Alexander, C. I. 1934a. Ostracoda of the genera Monoceratina and Orthonotacythere from the Cretaceous of Texas. Journal of Paleontology 8:57–67.Google Scholar
Alexander, C. I. 1934b. Ostracoda of the Midway (Eocene) of Texas. Journal of Paleontology 8:206–237.Google Scholar
Alexander, C. I. 1936. Ostracoda of the genera Eucythere, Cytherura, Eucytherura, and Loxoconcha from the Cretaceous of Texas. Journal of Paleontology 10:689–694.Google Scholar
Alexander, C. I., and Alexander, C. W.. 1933. Reversal of valve size and hinge structure in a species of the genus Cytheridea . American Midland Naturalist 14:280–283.Google Scholar
Andersson, M. 1994. Sexual selection. Princeton Unversity Press, Princeton, N.J.CrossRefGoogle Scholar
Arnqvist, G. 1998. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393:784–786.Google Scholar
Astrop, T. I., Park, L. E., Brown, B., and Weeks, S. C.. 2012. Sexual discrimination at work: spinicaudatan ‘clam shrimp’ (Crustacea: Branchiopoda) as a model organism for the study of sexual system evolution. Palaeontologia Electronica 15(2).Google Scholar
Athersuch, J., Horne, D. J., and Whittaker, J. E.. 1989. Marine and brackish water ostracods. Bath Press, Avon, UK.Google Scholar
Berry, E. W. 1925. Upper Cretaceous ostracoda from Maryland. American Journal of Science 9:481–487.CrossRefGoogle Scholar
Blanckenhorn, W. U., Meier, R., and Teder, T.. 2007. Rensch’s rule in insects: pattens among and within species. Pp. 60–70 in D. J. Fairbairn, W. U. Blanckenhorn, and T. Székely, eds. Sex, size and gender roles. Oxford University Press, Oxford.Google Scholar
Bonnema, J. H. 1940. Ostracoden aus der Kreide des Untergrundes der nordoestlichen Niederlande. Naturhistorisch Maandblad 30.Google Scholar
Brouwers, E. M., and Hazel, J. E.. 1978. Ostracoda and correlation of the Severn Formation (Navarroan; Maestrichtian) of Maryland. Journal of Paleontology 52(Suppl. to No. 6):1–52.Google Scholar
Brouwers, E. M., and Hazel, J. E.. 1980. Eucytherl sohli, a new name for Eucythere alexanderi Brouwers and Hazel, 1978. Journal of Paleontology 54:1352–1352.Google Scholar
Brown, P. M. 1957. Upper Cretaceous Ostracoda from North Carolina. North Carolina Department of Conservation and Development Bulletin 70:1–27.Google Scholar
Bush, A., Powell, M. G., Arnold, W. S., Bert, T. M., and Daley, G. M.. 2002. Time-averaging, evolution and morphological variation. Paleobiology 28:9–25.2.0.CO;2>CrossRefGoogle Scholar
Butler, E. A., and Jones, D. E.. 1957. Cretaceous Ostracoda of Prothrop and Rayburns salt domes Bienville Parish, Louisiana. Louisiana Geological Society Geological Bulletins 32:1–65.Google Scholar
Butlin, R., Schön, I., and Martins, K.. 1998. Asexual reproduction in nonmarine ostracods. Heredity 81:473–480.Google Scholar
Cederstrom, P., Ahlberg, P., Nilsson, C. H., Ahlgren, J., and Eriksson, M. E.. 2011. Moulting, ontogeny and sexual dimorphism in the Cambrian ptychopariid trilobite Strenuaeva inflata from the northern Swedish Caledonides. Palaeontology 54:685–703.CrossRefGoogle Scholar
Chapman, R. E., Galton, P. M., Sepkoski, J. J., and Wall, W. P.. 1981. A morphometric study of the cranium of the pachycephalosaurid dinosaur Stegoceras . Journal of Paleontology 55:608–618.Google Scholar
Cohen, A. C., and Morin, J. G.. 1990. Patterns of reproduction in ostracodes: a review. Journal of Crustacean Biology 10:184–211.Google Scholar
Crane, M. J. 1965. Upper Cretaceous ostracodes of the Gulf Coast area. Micropaleontology 11:191–254.Google Scholar
Dale, J., Dunn, P. O., Figuerola, J., Lislevand, T., Szekely, T., and Whittingham, L. A.. 2007. Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proceedings of the Royal Society of London B 274:2971–2979.Google ScholarPubMed
Danielopol, D. L. 1980. On the carapace shape of some European freshwater interstitial Candoninae (Ostracoda). Proceedings of the Biological Society of Washington 93:743–756.Google Scholar
Darwin, C. 1871. The descent of man, and selection in relation to sex. John Murray, London.Google Scholar
Doherty, P. F., Sorci, G., Royle, J. A., Hines, J. E., Nichols, J. D., and Boulinier, T.. 2003. Sexual selection affects local extinction and turnover in bird communities. Proceedings of the National Academy of Sciences USA 100:5858–5862.CrossRefGoogle ScholarPubMed
Dunn, P. O., Whittingham, L. A., and Pitcher, T. E.. 2001. Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55:161–175.Google ScholarPubMed
Emlen, D. J., Marangelo, J., Ball, B., and Cunningham, C. W.. 2005. Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060–1084.Google Scholar
Fairbairn, D. J. 2007. Introduction: the enigma of sexual size dimorphism. Pp. 1–12 in D. J. Fairbairn, W. U. Blanckenhorn, and T. Székely, eds. Sex, size and gender roles. Oxford University Press, Oxford.Google Scholar
Fairbairn, D. J., Blanckenhorn, W. U., and Székely, T. eds. 2007. Sex, size and gender roles. Oxford University Press, Oxford.CrossRefGoogle Scholar
Fortey, R. A., and Hughes, N. C.. 1998. Brood pouches in trilobites. Journal of Paleontology 72:638–649.Google Scholar
Fraley, C., Raftery, A., Murphy, B., and Scrucca, L.. 2012). mclust version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation. Technical Report 597. Department of Statistics, University of Washington, Seattle, Wash.Google Scholar
Fraley, C., and Raftery, A. E.. 2002. Model-based clustering, discriminant analysis and density estimation. Journal of the American Statistical Association 97:611–631.CrossRefGoogle Scholar
Fraley, C., and Raftery, A. E.. 2007. Bayesian regularization for normal mixture estimation and model-based clustering. Journal of Classification 24:155–181.Google Scholar
Gage, M. J. G., Parker, G. A., Nylin, S., and Wiklund, C.. 2002. Sexual selection and speciation in mammals, butterflies and spiders. Proceedings of the Royal Society of London B 269:2309–2316.Google Scholar
Gingerich, P. D. 1981. Variation, sexual dimorphism, and social structure in the Early Eocene horse Hyracotherium (Mammalia, Perissodactyla). Paleobiology 7:443–455.CrossRefGoogle Scholar
Gosden, T. P., Shastri, K. L., Innocenti, P., and Chenoweth, S. F.. 2012. The B-matrix harbors significant and sex-specific constraints on the evolution of multicharacter sexual dimorphism. Evolution 66:2106–2116.CrossRefGoogle ScholarPubMed
Hazel, J. E., and Paulson, O. L.. 1964. Some new ostracode species from the Austinian and Tayloran (Coniacian and Campanian) rocks of the East Texas Embayment. Journal of Paleontology 38:1047–1064.Google Scholar
Hill, B. L. 1954. Reclassification of winged Cythereis and winged Brachycythere . Journal of Paleontology 28:804–826.Google Scholar
Hirst, A. G., and Kiorboe, T.. 2014. Macroevolutionary patterns of sexual size dimorphism in copepods. Proceedings of the Royal Society of London B 281(1791):20140739.Google Scholar
Horne, D. J., Baltanás, A., and Paris, G.. 1998a. Geographical distribution of reproductive modes in living ostracods. Pp. 77–99 in K. Martens, ed. Sex and parthenogenesis: evolutionary ecology of reproductive modes in non-marine ostracods. Backhuys, Leiden.Google Scholar
Horne, D. J., Danielopol, D. L., and Martens, K.. 1998b. Reproductive behavior. Pp. 157–195 in K. Martens, ed. Sex and parthenogenesis: evolutionary ecology of reproductive modes in non-marine ostracods. Backhuys, Leiden.Google Scholar
Howe, H. V., and Laurencich, L.. 1958. Introduction to the study of Cretaceous Ostracoda. Louisiana State University Press, Baton Rouge.Google Scholar
Hunt, G. 2004. Phenotypic variance inflation in fossil samples: an empirical assessment. Paleobiology 30:487–506.2.0.CO;2>CrossRefGoogle Scholar
Ikeya, N., and Ueda, H.. 1988. Morphological variations of Cytheromorpha acupunctata (Brady) in continuous populations at Hamana-ko Bay, Japan. Pp. 319–340 in T. Hanai, N. Ikeya, and K. Ishizaki, eds. Evolutionary biology of Ostracoda. Elsevier, Kodansha, Japan.Google Scholar
Israelsky, M. C. 1929. Upper Cretaceous Ostracoda of Arkansas. Arkansas Geological Survey Bulletin 2:1–28.Google Scholar
Jennings, P. H. 1936. A microfauna from the Monmouth and basal Rancocos of New Jersey. Bulletins of American Paleontology 23(78):159–234.Google Scholar
Johnstone, R. A. 1995. Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biological Reviews of the Cambridge Philosophical Society 70(1):1–65.Google Scholar
Kamiya, T. 1992. Heterochronic dimorphism of Loxoconcha uranouchiensis (Ostracoda) and its implications for speciation. Paleobiology 18:221–236.Google Scholar
Karubian, J., and Swaddle, J. P.. 2001. Selection on females can create “larger males.”. Proceedings of the Royal Society of London B 268:725–728.Google Scholar
Knell, R. J., Naish, D., Tomkins, J. L., and Hone, D. W. E.. 2013. Sexual selection in prehistoric animals: detection and implications. Trends in Ecology and Evolution 28:38–47.Google Scholar
Lü, J., Unwin, D. M., Deeming, D. C., Jin, X., Liu, Y., and Ji, Q.. 2011. An egg-adult association, gender, and reproduction in pterosaurs. Science 331:321–324.CrossRefGoogle ScholarPubMed
Makowski, H. 1962. Problem of sexual dimoprhism in ammonites. Palaeontologia Polonica 12:1–90.Google Scholar
Marsson, T. 1880. Die Cirripeden und Ostracoden der weißen Schreibkreide der Insel Ruegen. Naturwissenschaft, Neu-Pommern, Ruegen 12:1–50.Google Scholar
Martins, M. J., Hunt, G., Lockwood, R., Swaddle, J. P., and Horne, D. J.. 2017. Correlation between investment in sexual traits and valve sexual dimorphism in Cyprideis species (Ostracoda). PLoS ONE 12:e0177791.Google Scholar
Matzke-Karasz, R., Neil, J. V., Smith, R. J., Symonova, R., Morkovsky, L., Archer, M., Hand, S. J., Cloetens, P., and Tafforeau, P.. 2014. Subcellular preservation in giant ostracod sperm from an early Miocene cave deposit in Australia. Proceedings of the Royal Society of London B 281(1786):20140394.Google ScholarPubMed
Morrow, E. H., and Pitcher, T. E.. 2003. Sexual selection and the risk of extinction in birds. Proceedings of the Royal Society of London B 270:1793–1799.Google Scholar
Ozawa, H. 2013. The history of sexual dimorphism in Ostracoda (Arthropoda, Crustacea) since the Palaeozoic. Pp. 51–80 in H. Moriyama, ed. Sexual dimorphism. InTech, Rijeka, Croatia.Google Scholar
Price, J. J., Lanyon, S. M., and Omland, K. E.. 2009. Losses of female song with changes from tropical to temperate breeding in the New World blackbirds. Proceedings of the Royal Society of London B 276:1971–1980.Google Scholar
Puckett, T. M. 1994. New Ostracoda species from an Upper Cretaceous oyster reef, northern Gulf Coastal Plain, USA. Journal of Paleontology 68:1321–1335.Google Scholar
Puckett, T. M. 1996. Ecological atlas of Upper Cretaceous ostracodes of Alabama. Geological Survey of Alabama Monograph 14:1–176.Google Scholar
Puckett, T. M. 2002. Systematics and paleobiogeography of brachycytherine Ostracoda. Micropaleontology 48:1–87.Google Scholar
Rohlf, F. J. 2013. tpsDIG, version 2.17. SUNY Stonybrook. http://life.bio.sunysb.edu/morph.Google Scholar
Schmidt, R. A. M. 1948. Ostracoda from the Upper Cretaceous and Lower Eocene of Maryland, Delaware, and Virginia. Journal of Paleontology 22:389–431.Google Scholar
Shine, R. 1989. Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Quarterly Review of Biology 64:419–461.CrossRefGoogle ScholarPubMed
Siveter, D. J., Sutton, M. D., Briggs, D. E. G., and Siveter, D. J.. 2003. An ostracode crustacean with soft parts from the Lower Silurian. Science 302:1749–1751.CrossRefGoogle ScholarPubMed
Skinner, H. C. 1956. Ostracoda from basal Arkadelphia Marl exposures near Hope, Arkansas. Transactions of the Gulf Coast Association of Geological Societies 6:179–204.Google Scholar
Smith, J. K. 1978. Ostracoda of the Prairie Bluff Chalk, Upper Cretaceous, (Maestrichtian) and the Pine Barren Member of the Clayton Formation, Lower Paleocene (Danian) from exposures along Alabama State Highway 263 in Lowndes County, Alabama. Transactions of the Gulf Coast Association of Geological Societies 28:539–579.Google Scholar
Swain, F. M. 1948. Ostracoda in Cretaceous and Tertiary subsurface geology. Maryland Department of Geology, Mines, and Water Resources Bulletin 2:187–212.Google Scholar
Swain, F. M. 1952. Ostracoda from wells in North Carolina: Part 2. Mesozoic Ostracoda. United States Geological Survey Professional Paper 234-B:59–93.CrossRefGoogle Scholar
Swain, F. M., and Brown, P. M.. 1964. Cretaceous Ostracoda from wells in the southeastern United States. North Carolina Department of Conservation and Development Bulletin 78:1–55.Google Scholar
van Harten, D. 1983. Resource competition as a possible cause of sex ratio in benthic ostracodes. Pp. 568–580 in R. F. Maddocks, ed. Applications of Ostracoda. Department of Geosciences, University of Houston, Houston, Tex.Google Scholar
van Morkhoven, F. P. C. M. 1962. Post-Paleozoic Ostracoda. Elsevier, Amsterdam.Google Scholar
Van Valkenburgh, B., and Sacco, T.. 2002. Sexual dimorphism, social behavior, and intrasexual competition in large Pleistocene carnivorans. Journal of Vertebrate Paleontology 22:164–169.Google Scholar
Vandekerkhove, J., Matzke-Karasz, R., Mezquita, F., and Rossetti, G.. 2007. Experimental assessment of the fecundity of Eucypris virens (Ostracoda, Crustacea) under natural sex ratios. Freshwater Biology 52:1058–1064.Google Scholar