The evolution of copulation frequency and the mechanisms of reproduction in male Anolis lizards

The evolution of many morphological structures is associated with the behavioral context of their use, particularly for structures involved in copulation. Yet, few studies have considered evolutionary relationships among the integrated suite of structures associated with male reproduction. In this study, we examined nine species of lizards in the genus Anolis to determine whether larger copulatory morphologies and higher potential for copulatory muscle performance evolved in association with higher copulation rates. In 10–12 adult males of each species, we measured the size of the hemipenes and related muscles, the seminiferous tubules in the testes, and the renal sex segments in the kidneys, and we assessed the fiber type composition of the muscles associated with copulation. In a series of phylogenetically-informed analyses, we used field behavioral data to determine whether observed rates of copulation were associated with these morphologies.We found that species with larger hemipenes had larger fibers in the RPM (the retractor penis magnus, a muscle that controls hemipenis movement), and that the evolution of larger hemipenes and RPM fibers is associated with the evolution of higher rates of copulatory behavior. However, the sizes of the seminiferous tubules and renal sex segments, and the muscle fiber composition of the RPM, were not associated with copulation rates. Further, body size was not associated with the size of any of the reproductive structures investigated. The results of this study suggest that peripheral morphologies involved in the transfer of ejaculate may be more evolutionarily labile than internal structures involved in ejaculate production [Current Zoology 60 (6): 768–777, 2014].

[1]  M. Cohn,et al.  Evolution of External Genitalia: Insights from Reptilian Development , 2014, Sexual Development.

[2]  J. L. Tomkins,et al.  Female monopolization mediates the relationship between pre- and postcopulatory sexual traits , 2014, Nature Communications.

[3]  Michele A Johnson,et al.  Colorful displays signal male quality in a tropical anole lizard , 2013, Naturwissenschaften.

[4]  L. Simmons,et al.  Sperm wars and the evolution of male fertility. , 2012, Reproduction.

[5]  D. Rabosky,et al.  Equilibrium speciation dynamics in a model adaptive radiation of island lizards , 2010, Proceedings of the National Academy of Sciences.

[6]  J. Losos,et al.  BEHAVIORAL CONVERGENCE AND ADAPTIVE RADIATION: EFFECTS OF HABITAT USE ON TERRITORIAL BEHAVIOR IN ANOLIS LIZARDS , 2009, Evolution; international journal of organic evolution.

[7]  J. Hicks,et al.  Exhaustive exercise training enhances aerobic capacity in American alligator (Alligator mississippiensis) , 2009, Journal of Comparative Physiology B.

[8]  J. Wade,et al.  Androgen dependent seasonal changes in muscle fiber type in the dewlap neuromuscular system of green anoles , 2007, Physiology & Behavior.

[9]  Robert E. Wilson,et al.  Reconstructing the environment in Iraq. , 2004, Environmental health perspectives.

[10]  J. Wade,et al.  Courtship and copulation in the adult male green anole: Effects of season, hormone and female contact on reproductive behavior and morphology , 2007, Behavioural Brain Research.

[11]  Kate E. Jones,et al.  Mating system and brain size in bats , 2006, Proceedings of the Royal Society B: Biological Sciences.

[12]  J. Wade Current research on the behavioral neuroendocrinology of reptiles , 2005, Hormones and Behavior.

[13]  D. Sever,et al.  Renal sexual segment of the ground skink, Scincella laterale (Reptilia, Squamata, Scincidae) , 2005, Journal of morphology.

[14]  J. Wade,et al.  Testosterone Regulates Androgen Receptor Immunoreactivity in the Copulatory, but not Courtship, Neuromuscular System in Adult Male Green Anoles , 2005, Journal of neuroendocrinology.

[15]  J. Wade,et al.  Normally occurring intersexuality and testosterone induced plasticity in the copulatory system of adult leopard geckos , 2005, Hormones and Behavior.

[16]  J. Wade,et al.  Seasonal plasticity in the copulatory neuromuscular system of green anole lizards: a role for testosterone in muscle but not motoneuron morphology. , 2004, Journal of neurobiology.

[17]  J. Wade,et al.  Fiber Type Composition of the Muscle Responsible for Throat Fan Extension in Green Anole Lizards , 2004, Brain, Behavior and Evolution.

[18]  D. Hosken,et al.  Sexual selection and genital evolution. , 2004, Trends in ecology & evolution.

[19]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[20]  L. Simmons,et al.  Sperm competition selects for increased testes mass in Australian frogs , 2002 .

[21]  J. Wade,et al.  Sexual dimorphisms in a copulatory neuromuscular system in the green anole lizard , 2002, The Journal of comparative neurology.

[22]  J. Wade Zebra finch sexual differentiation: The aromatization hypothesis revisited , 2001, Microscopy research and technique.

[23]  R. Shine,et al.  Are snakes right-handed ? Asymmetry in hemipenis size and usage in gartersnakes (Thamnophis sirtalis) , 2000 .

[24]  A. Arnold,et al.  Sexual differentiation of the zebra finch song system: positive evidence, negative evidence, null hypotheses, and a paradigm shift. , 1997, Journal of neurobiology.

[25]  A. Purvis,et al.  Sperm competition: mating system, not breeding season, affects testes size of primates , 1995 .

[26]  M. Gage Associations between body size, mating pattern, testis size and sperm lengths across butterflies , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  T. Garland,et al.  Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts , 1992 .

[28]  A. Bass Sounds from the Intertidal Zone: Vocalizing FishSex and species differences in the coadaptation of behavior and neural mechanisms in a simple motor system , 1990 .

[29]  T. Birkhead Sperm competition in birds. , 1998, Reviews of reproduction.

[30]  D. Kelley,et al.  The sexually dimorphic larynx of Xenopus laevis: development and androgen regulation. , 1986, The American journal of anatomy.

[31]  E. N. Arnold The hemipenis of lacertid lizards (Reptilia: Lacertidae): structure, variation and systematic implications , 1986 .

[32]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[33]  J. Stamps 9. SEXUAL SELECTION, SEXUAL DIMORPHISM, AND TERRITORIALITY , 1983 .

[34]  D. Crews Hemipenile Preference: Stimulus Control of Male Mounting Behavior in the Lizard Anolis carolinensis , 1978, Science.

[35]  L. Guth,et al.  Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle. , 1969, Experimental neurology.

[36]  J. Savage,et al.  A guide to the snake hemipenis: a survey of basic structure and systematic characteristics , 1960, Zoologica : scientific contributions of the New York Zoological Society..

[37]  R. Snyder,et al.  The anatomy and function of the pelvic girdle and hindlimb in lizard locomotion. , 1954, The American journal of anatomy.

[38]  B. Roy,et al.  Hormonal Regulation of Testicular Functions in Reptiles , 2011 .

[39]  D. Gist Hormones and the Sex Ducts and Sex Accessory Structures of Reptiles , 2011 .

[40]  T. Birkhead,et al.  Testes size in birds: quality versus quantity—assumptions, errors, and estimates , 2007 .

[41]  R. Jones Evolution of the vertebrate epididymis. , 1998, Journal of reproduction and fertility. Supplement.

[42]  R. Tokarz MATE CHOICE IN LIZARDS: A REVIEW , 1995 .

[43]  D. Crews Interrelationships Among Ecological, Behavioral, and Neuroendocrine Processes in the Reproductive Cycle of Anolis Carolinensis and Other Reptiles , 1980 .

[44]  M. Prasad,et al.  Physiology of the sexual segment of the kidney in reptiles , 1972 .