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Evolution of body mass in the Pan-Alcidae (Aves, Charadriiformes): the effects of combining neontological and paleontological data

  • N. Adam Smith (a1) (a2)

Hypotheses regarding the evolution of many clades are often generated in the absence of data from the fossil record and potential biases introduced by exclusion of paleontological data are frequently ignored. With regard to body size evolution, extinct taxa are frequently excluded because of the lack of body mass estimates—making identification of reliable clade specific body mass estimators crucial to evaluating trends on paleontological timescales. Herein, I identify optimal osteological dimensions for estimating body mass in extinct species of Pan-Alcidae (Aves, Charadriiformes) and utilize newly generated estimates of body mass to demonstrate that the combination of neontological and paleontological data produces results that conflict with hypotheses generated when extant species data are analyzed in isolation. The wing-propelled diving Pan-Alcidae are an ideal candidate for comparing estimates of body mass evolution based only on extant taxa with estimates generated including fossils because extinct species diversity (≥31 species) exceeds extant diversity, includes examples from every extant genera, and because phylogenetic hypotheses of pan-alcid relationships are not restricted to the 23 extant species. Phylogenetically contextualized estimation of body mass values for extinct pan-alcids facilitated evaluation of broad scale trends in the evolution of pan-alcid body mass and generated new data bearing on the maximum body mass threshold for aerial flight in wing-propelled divers. The range of body mass in Pan-Alcidae is found to exceed that of all other clades of Charadriiformes (shorebirds and allies) and intraclade body mass variability is recognized as a recurring theme in the evolution of the clade. Finally, comparisons of pan-alcid body mass range with penguins and the extinct †Plotopteridae elucidate potentially shared constraints among phylogenetically disparate yet ecologically similar clades of wing-propelled divers.

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Ainley, D. G. 1990. Farallon seabirds: patterns at the community level. In D. G. Ainley, and R. J. Boekelheide, eds. Seabirds of the Farallon Islands: ecology, dynamics, and structure of an upwelling-system community. Stanford University Press, Stanford.
Ainley, D. G., Strong, C. S., Penniman, T. M., and Boekelheide, R. J. 1990. The feeding ecology of Farallon seabirds. Pp. 51127. in D. G. Ainley, and R. J. Boekelheide, eds. Seabirds of the Farallon Islands: ecology, dynamics, and structure of an upwelling-system community. Stanford University Press, Stanford, CA.
Anderson, J. F., Rahn, H., and Prange, H. D. 1979. Scaling of Supportive Tissue Mass. Quarterly Review of Biology 54:139148.
Ando, T., and Fordyce, R. E. 2013. Evolutionary drivers for flightless, wing-propelled divers in the Northern and Southern Hemispheres. Palaeogeography Palaeoclimatology Palaeoecology 400:5061.
Ashmole, N. P. 1968. Body Size Prey Size and Ecological Segregation in 5 Sympatric Tropical Terns (Aves Laridae). Systematic Zoology 17:292304.
Barrett, R. T., Anker-Nielsen, T., and Krasov, Y. V. 1997. Can Norwegian and Russian Razorbills Alca torda be identified by their measurements? Marine Ornithology 25:58.
Bedard, J. 1985. Evolution and characteristics of the Atlantic Alcidae. Pp. 150in D. N. Nettleship, and T. R. Birkhead, eds. The Atlantic Alcidae: the evolution, distribution, and biology of the auks inhabiting the Atlantic Ocean and adjacent water areas. Academic Press, London.
Bergmann, C. 1847. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien 3:595708.
Birkhead, T. R. 1993. Great Auk Islands: a field biologist in the Arctic. Poyser, London.
Blackburn, T. M., and Gaston, K. J. 1994. The Distribution of Body Sizes of the Worlds Bird Species. Oikos 70:127130.
Blackburn, T. M., and Gaston, K. J.. 1996. Spatial patterns in the body sizes of bird species in the New World. Oikos 77:436446.
Boessenecker, R. W., and Smith, N. A. 2011. Latest Pacific Basin record of a bony-toothed bird (Aves, Pelagornithidae) from the Pliocene Purisima Formation of California, USA. Journal of Vertebrate Paleontology 31:652657.
Campbell, K. E. Jr., and Marcus, L. 1992. The relationship of hindlimb bone dimensions to body weight in birds. Science Series. Natural History Museum of Los Angeles County 36:395412.
Campione, N. E., and Evans, D. C. 2012. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10:60 doi: 10.1186/1741-7007-10-60.
Chandler, R. M. 1990. Fossil birds of the San Diego Formation, Late Pliocene, Blancan, San Diego County California. Ornithological Monographs 44:73161.
Cope, E. D. 1887. The Origin of the Fittest. Appleton, New York.
Dunning, J. B. J. 2008. CRC Handbook of Avian Body Masses, 2nd Ed. CRC Press, Boca Raton.
Dyke, G. J., Wang, X., and Habib, M. B. 2011. Fossil Plotopterid Seabirds from the Eo-Oligocene of the Olympic Peninsula (Washington State, USA): Descriptions and Functional Morphology. Plos One 6:e25672 doi: 10.1371/journal.pone.0025672.
Elliott, K. H., Ricklefs, R. E., Gaston, A. J., Hatch, S. A., Speakman, J. R., and Davoren, G. K. 2013. High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins. Proceedings of the National Academy of Sciences of the USA 110:93809384.
Etienne, R. S., and Apol, M. E. 2009. Estimating speciation and extinction rates from diversity data and the fossil record. Evolution 63:244255.
Field, D. J., Lynner, C., Brown, C., and Darroch, S. A. F. 2013. Skeletal correlates for body mass estimation in modern and fossil flying birds. Plos One 8:e82000 doi:10.1371/journal.pone.0082000.
Fuller, E. 1999. The Great Auk. Errol Fuller, Kent, England.
Grafen, A. 1989. The phylogenetic regression. Philosophical Transactions of the Royal Society of London B 326:119157.
Gryz, P. K. 2013. Tajemnice ewolucji alk. Kosmos 62:443454.
Habib, M. 2010. The structural mechanics and evolution of aquaflying birds. Biological Journal of the Linnean Society 99:687698.
Hackett, S., Kimball, R., Reddy, S., Bowie, R., Braun, E., Braun, M., Chojnowski, J., Cox, W., Han, K., and Harshman, J. 2008. A phylogenomic study of birds reveals their evolutionary history. Science 320:1763.
Hardin, G. 1960. The competitive exclusion principle. Science 131:12921297.
Harvey, P. H., and Pagel, M. D. 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
Hipfner, J. M., and Greenwood, J. M.. 2008. Breeding biology of the Common Murre at Triangle Island, British Columbia, Canada, 2002–2007. Northwestern Naturalist 89:7684.
Hurvich, C. M., and Tsai, C. L.. 1989. Regression and Time-Series Model Selection in Small Samples. Biometrika 76:297307.
Jadwiszczak, P. 2001. Body size of Eocene antarctic penguins. Polish Polar Research 22:147158.
Kawano, T., and Kawano, S. 2001. A large plotopterid (penguin-like bird) fossil from Sakido-cho, Nagasaki Prefecture. P. abstract no. 60. 150th Regular Meeting of the Paleontological Society of Japan. Iwai, Ibaraki Prefecture.
Kovacs, C. E., and Meyers, R. A. 2000. Anatomy and Histochemistry of Flight Muscles in a Wing-Propelled Diving Bird, the Atlantic Puffin, Fratercula arctica. Journal of Morphology 244:109125.
Ksepka, D. T. 2014. Flight performance of the largest volant bird. Proceedings of the National Academy of Sciences of the United States of America 111:1062410629.
Ksepka, D. T., Fordyce, R. E., Ando, T., and Jones, C. M. 2012. New Fossil Penguins (Aves, Sphenisciformes) from the Oligocene of New Zealand Reveal the Skeletal Plan of Stem Penguins. Journal of Vertebrate Paleontology 32:235254.
Livezey, B. C. 1989. Morphometric Patterns in Recent and Fossil Penguins (Aves, Sphenisciformes). Journal of Zoology 219:269307.
Macarthur, R., and Levins, R. 1967. The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist 101:377385.
Martins, E. P., and Hansen, T. F. 1997. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist 149:646667.
Maurer, B. A. 2013. Geographic variation in body size distributions of continental avifauna. Pp. 8394in F. A. Smith, and S. K. Lyons, eds. Animal Body Size: Linking pattern and process across space time and taxonomic group. University of Chicago Press, Chicago.
Mayr, G. 2009. Paleogene fossil birds. Springer, Heidelberg.
Mayr, G., and Clarke, J. 2003. The deep divergences of neornithine birds: a phylogenetic analysis of morphological characters. Cladistics 19:527553.
McClain, C. R., and Boyer, A. G. 2009. Biodiversity and body size are linked across metazoans. Proceedings of the Royal Society B 276:22092215.
McCormack, J. E., Harvey, M. G., Faircloth, B. C., Crawford, N. G., Glenn, T. C., and Brumfield, R. T. 2013. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. Plos One 8:e54848 doi:10.1371/journal.pone.0054848.
Norell, M. A. 1992. The effect of phylogeny on temporal diversity and evolutionary tempo. Pp. 89118in M. J. Novacek, and Q. D. Wheeler, eds. Extinction and Phylogeny. Columbia University Press, New York.
Olson, S. L. 1985. The fossil record of birds. Pp. 79252in D. S. Farmer, and A. King, eds. Avian Biology. Academic Press, Florida.
Olson, S. L., and Hasegawa, Y. 1979. Fossil Counterparts of Giant Penguins from the North Pacific. Science 206:688689.
Olson, S. L., and Hasegawa, Y.. 1996. A new genus and two new species of gigantic plotopteridae from Japan. Journal of Vertebrate Paleontology 16:742751.
Omerod, S., and Tyler, S. 2005. Family Cinclidae. P. 895in J. del Hoyo, A. Elliott, and D. A. Christie, eds. Handbook of the Birds of the World Vol. 10. Cuckoo-shrikes to Thrushes. Lynx Edicions, Barcelona.
Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., and Pearse, W. 2011. Caper: Comparative Analyses of Phylogenetics and Evolution in R. R package version 0.5.
Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877884.
Paradis, E., Claude, J., and Strimmer, K. 2004. Ape: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289.
Parham, J. F., Donoghue, P. C. J., Bell, C. J., Calway, T. D., Head, J. J., Holroyd, P. A., Inoue, J. G., Irmis, R. B., Joyce, W. G., Ksepka, D. T., Patane, J. S. L., Smith, N. D., Tarver, J. E., van Tuinen, M., Yang, Z. H., Angielczyk, K. D., Greenwood, J. M., Hipsley, C. A., Jacobs, L., Makovicky, P. J., Muller, J., Smith, K. T., Theodor, J. M., Warnock, R. C. M., and Benton, M. J. 2012. Best Practices for Justifying Fossil Calibrations. Systematic Biology 61:346359.
Pyron, R. A. 2011. Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Systematic Biology 60:466481.
R Development Core Team. 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Rabosky, D. L. 2010. Extinction Rates Should Not Be Estimated from Molecular Phylogenies. Evolution 64:18161824.
Rahn, H., Paganelli, C. V., and Ar, A. 1975. Relation of Avian Egg Weight to Body-Weight. Auk 92:750765.
Revell, L. J. 2010. Phylogenetic signal and linear regression on species data. Methods in Ecology and Evolution 1:319329.
Revell, L. J. 2012. phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217223.
Serrano, F. J., Palmqvist, P., and Sanz, J. L. 2015. Multivariate analysis of neognath skeletal measurements: implications for body mass estimation in Mesozoic birds. Zoological Journal of the Linnean Society 173:929955.
Shaul, S., and Graur, D. 2002. Playing chicken (Gallus gallus): methodological inconsistencies of molecular divergence date estimates due to secondary calibration points. Gene 300:5961.
Simpson, G. G. 1946. Fossil Penguins. Bulletin of the American Museum of Natural History 87:199.
Slater, G. J., Harmon, L. J., and Alfaro, M. E. 2012. Integrating Fossils with Molecular Phylogenies Improves Inference of Trait Evolution. Evolution 66:39313944.
Smith, F. A., and Lyons, S. K. 2013. Animal Body Size: Linking Pattern and Process Across Space. Time, and Taxonomic Group University of Chicago Press, Chicago.
Smith, F. A., Lyons, S. K., Jones, K. E., Maurer, B. A., and Brown, J. H. 2013. The influence of flight on patterns of body size diversity and heritability. Pp. 187205in F. A. Smith, and S. K. Lyons, eds. Animal Body Size: Linking pattern and process across space time and taxonomic group. University of Chicago Press, Chicago.
Smith, N. A. 2011a. Systematics and evolution of extinct and extant Pan-Alcidae (Aves, Charadriiformes): combined phylogenetic analyses, divergence estimation, and paleoclimatic interactions. Ph.D. dissertation. University of Texas at Austin.
Smith, N. A. 2011b. Taxonomic revision and phylogenetic analysis of the flightless Mancallinae (Aves, Pan-Alcidae). ZooKeys 91:1116.
Smith, N. A. 2013. A new species of auk (Charadriiformes, Pan-Alcidae) from the Miocene of Mexico. Condor 115:7783.
Smith, N. A. 2014. The fossil record and phylogeny of the auklets (Pan-Alcidae, Aethiini). Journal of Systematic Palaeontology 12:217236.
Smith, N. A. 2015. Sixteen vetted fossil calibrations for divergence dating of Charadriiformes (Aves, Neognathae). Palaeontologia Electronica 1470 18.1.4FC, 118.
Smith, N. A., and Clarke, J. A. 2011. An alphataxonomic revision of extinct and extant razorbills (Aves, Alcidae): a combined morphometric and phylogenetic approach. Ornithological Monographs 72:161.
Smith, N. A., and Clarke, J. A.. 2012. Endocranial anatomy of the Charadriiformes: sensory system variation and the evolution of wing-propelled diving. Plos One 7:e49584 doi: 10.1371/journal.pone.0049584.
Smith, N. A., and Clarke, J. A.. 2014. Osteological histology of the Pan-Alcidae (Aves, Charadriiformes): correlates of wing-propelled diving and flightlessness. The Anatomical Record 297:188199.
Smith, N. A., and Clarke, J. A.. 2015. Systematics and evolution of the Pan-Alcidae (Aves, Charadriiformes). Journal of Avian Biology 46:125140.
Stewart, J. R. 2007. An evolutionary study of some archaeologically significant avian taxa in the quaternary of the western Palaearctic. Archaeopress, Oxford.
Storer, R. W. 1960. Evolution in the diving birds. Pp. 694707in G. Bergman, K. O. Donner, and L. Haartman, eds. International Ornithogical Congress. Tilgmannin Kirjapaino.
Warheit, K. I., and Lindberg, D. R. 1988. Interactions between seabirds and marine mammals through time: interference competition at breeding sites. Pp. 292328in J. Burger, ed. Seabirds and Other Marine Vertebrates: Competition, Predation, and Other Interactions. Columbia University Press, New York.
Whitlock, M. C., and Schluter, D. 2008. The analysis of biological data, 2nd Edition. Roberts and Company Publishers, Greenwood Village, Colorado.
Wiens, J. J. 2009. Paleontology, genomics, and combined-data phylogenetics: can molecular data improve phylogeny estimation for fossil taxa? Systematic Biology 58:8799.
Wiens, J. J., Kuczynski, C. A., Townsend, T., Reeder, T. W., Mulcahy, D. G., and Sites, J. W. 2010. Combining phylogenomics and fossils in higher-level squamate reptile phylogeny: molecular data change the placement of fossil taxa. Systematic Biology 59:674688.
Wojczulanis-Jakubas, K., Jakubas, D., Welcker, J., Harding, A. M. A., Karnovsky, N. J., Kidawa, D., Steen, H., Stempniewicz, L., and Camphuysen, C. J. 2010. Body size variation of a high-Arctic seabird: the dovekie (Alle alle). Polar Biology 34:847854.
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