Abstract
Incorporating microsatellite techniques to determine parentage is a powerful addition to behavioral mating system studies in wild animals. Nonetheless, in some tetrapod taxa such as lizards, there are relatively few direct comparisons of individual reproductive success measured genetically versus estimates based on behavioral interactions, especially in species where males and females do not maintain prolonged social contact. We combined observations of behavior with microsatellite analysis of parentage over ten seasons in male Collared Lizards, (Crotaphytus collaris), to test the extent to which the proportion of each female’s total courtship interactions with different males predicted the proportion of total offspring sired by those males (proportion of paternity). Territorial males (T-males) court females frequently. Non-territorial (NT) males on the other hand behave stealthily. This allows them to court females, albeit less frequently, while limiting attacks by T-males. Both T- and NT-males occupied habitats that varied in structural complexity which might influence which males court and sire offspring with individual females, therefore we included habitat type (simple vs. complex) and male social tactic as possible predictors in our test. Proportion of courtship by NT-males did not predict their proportion of paternity in either habitat type. Courtship by T-males was a strong predictor of paternity in simple habitats but not complex habitats. Our findings support the hypothesis that courtship is a more accurate predictor of T-male mating success in simple habitats, which is consistent with previous findings suggesting that reduced area and topographical heterogeneity, especially the absence of subsurface crevices in simpler habitats, makes it more economical for T-males to prevent surreptitious mating by NT-males. Our study, therefore, highlights the importance of considering possible effects of alternative social tactics and variation in environmental conditions when testing the accuracy of behaviorally based estimates of breeding relationships, especially in polygamous species with multiple paternity.


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References
Abell AJ (1997) Estimating paternity with spatial behaviour and DNA fingerprinting in the striped plateau lizard, Sceloporus virgatus (Phrynosomatidae). Behav Ecol Sociobiol 41:217–226
Abell AJ (1999) Variation in clutch size and offspring size relative to environmental conditions in the lizard Sceloporus virgatus. J Herpetol 33:173–180
Altmann J (1974) Observational study of behaviour: sampling methods. Behav 49:227–266
Baird TA (2004) Reproductive coloration in female collared lizards, Crotophytus collaris, stimulates courtship by males. Herpetol 60:337–348
Baird TA (2013a) Lizards and other reptiles as model systems for the study of contest behaviour. In: Hardy ICW, Briffa M (eds) Animal contests. Cambridge University Press, Cambridge, pp 258–286
Baird TA (2013b) Social life on the rocks: behavioural diversity and sexual selection in collared lizards. In: Lutterschmidt WI (ed) Reptiles in research: investigations of ecology, physiology and behavior from desert to sea. Nova Science Publishers, Haupauge, pp 213–245
Baird TA (2018) Live fast and prosper: early territory defence is not costly in male collared lizards (Crotaphytus collaris). Biol J Linn Soc 123:628–635.
Baird TA, Timanus DK (1998) Social inhibition of territorial behaviour in yearling male collared lizards, Crotaphytus collaris. Anim Behav 56:989–994
Baird TA, Hews DK (2007) Homone levels in territorial and non-territorial male collared lizards. Physiol Behav 9:755–763
Baird TA, Curtis JL (2010) Context-dependent acquisition of territories by male collared lizards: the role of male mortality. Behav Ecol 21:753–763
Baird TA, York JR (2021) A decade of sexual selection studies reveals long-term patterns and processes of fitness variation in male collared lizards. Anim Behav 180:37–49
Baird TA, Acree MA, Sloan CL (1996) Age and gender-related differences in the social behavior and mating success of free-living collared lizards, Crotaphytus collaris. Copeia 1996:336–347
Baird TA, Sloan CL, Timanus DK (2001) Intra- and inter-seasonal variation in the socio-spatial behavior of adult male collared lizards, Crotaphytyus collaris (Reptilia, Crotaphytidae). Ethol 107:15–32
Baird TA, Timanus DK, Sloan CL (2003) Intra-and intersexual variation in social behavior. In: Fox SF, McCoy JK, Baird TA (eds). Johns Hopkins University Press, Baltimore, pp 7–46
Baird TA, Baird TD, Shine R (2020) War and peace: plasticity of aggression and the context of displays in male Australian Water Dragons. Evol Ecol 34:73–80
Best TL, Pfaffenberger GS (1987) Age and sexual variation in the diet of collared lizards (Crotaphytus collaris). Southwest Natur 32:415–421
Braun CA, Baird TA, York JR (2018) Behavioural plasticity in physically variable microhabitats: a field test of potential adaptive consequences in male collared lizards (Crotaphytus collaris). Biol J Linn Soc 125:37–49
Bull CM (1994) Population dynamics and pair fidelity in sleepy lizards. In: Vitt LJ, Pianka ER (eds) Lizard ecology: historical and experimental perspectives. Princeton University Press, pp 159–174
Bull CM, Freake MJ (1999) Home-range fidelity in the Australian sleepy lizard, Tiliqua rugosa. Aust J Zool 47:125–132
Bull CM, Cooper SJ, Baghurst BC (1998) Social monogamy and extra-pair fertilization in an Australian lizard, Tiliqua rugosa. Behav Ecol Sociobiol 44:63–72
Chapple DG, Keogh JS (2005) Complex mating system and dispersal patterns in a social lizard, Egernia whitii. Mol Ecol 14:1215–1227
Clutton-Brock TH, Parker GA (1995) Punishment in animal societies. Nature 373:209–216
Clutton-Brock T, Sheldon BC (2010) Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. TREE 25:562–573
Clutton-Brock T, Huchard E (2013) Social competition and selection in males and females. Phil Trans Roy Soc B: Biol Sci 368:20130074
Cooper W, Greenberg N (1992) Reptilian coloration and behavior. In: Gans C, Crews D (eds) Biology of the Reptilia. University of Chicago Press, Chicago, pp 298–422
Dyson ML, Reichert MS, Halliday TR (2013) Contests in amphibians. In: Hardy ICW, Briffa M (eds) Animal contests. Cambridge University Press, Cambridge, pp 228–257
Fox SF, McCoy JK, TA Baird (2003a) Lizard Social Behavior. Johns Hopkins University Press, Baltimore
Fox SF, McCoy JK, Baird TA (2003b) The evolutionary study of social behavior and the role of lizards as model organisms. In: Fox SF, McCoy JK, Baird TA (eds) Lizard social behavior. Johns Hopkins University Press, Baltimore, pp xi–xiv
Gardner MG, Bull CM, Cooper SJB (2002) High levels of genetic monogamy in the group-living Australian lizard Egernia stokesii. Mol Ecol 11:1787–1794
Gardner MG, Godfrey SS, Fenner AL, Donnelan SC, Bull CM (2012) Fine-scale spatial structuring as an inbreeding avoidance mechanism in the social skink Egernia stokesii. Aust J Zool 60:272–277
Gardner, MG, Pearson SK, Johnston GR, Schwarz MP (2015) Group living in squamate reptiles: a review of evidence for stable aggregations. Biol Rev 91:925–936
Gullberg A, Olsson M, Tegelström H (1997) Male mating success, reproductive success and multiple paternity in a natural population of sand lizards: behavioral and molecular genetics data. Mol Ecol 6:105–112
Hacking J, Stuart-Fox D, Gardner M (2017) Very low rates of multiple paternity detected in clutches for a wild agamid lizard. Aust J Zool 65:328–334
Haenel G, Smith LC, John-Alder HB (2003) Home-range analysis in Sceloporus undulatus II. A test of spatial relationships and reproductive success. Copeia 2003:113–123
Haynie ML, Van Den Bussche RA, Hoogland JL, Gilbert DA (2003) Parentage, multiple paternity, and breeding success in Gunnison’s and Utah prairie dogs. J Mamm 84:1244–1253
Hughes C (1998) Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecol 79:383–399
Husak JF, McCoy JK (2000) Diet composition of the collared lizard (Crotaphytus collaris) in west-central Texas. Tex J Sci 52:93–100
Hutchison DW, Strasburg JL, Brissom JA, Cummings S (2004) Isolation and characterization of 11 polymorphic microsatellite loci in collared lizards (Crotaphytus collaris). Mol Ecol Notes 4:554–556
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106
LeBas N (2001) Microsatellite determination of male reproductive success in a natural population of the territorial ornate dragon lizard, Ctenophorus ornatus. Mol Ecol 10:193–203
Marshall T, Slate J, Kruuk L, Pemberton J (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
McAlpin S, Duckett P, Stow A (2011) Lizards cooperatively tunnel to construct a long-term home for family members. PLoS ONE 6:e19041
Morrison SF, Keogh JS, Scott AW (2002) Molecular determination of paternity in a natural population of the multiple mating polygynous lizard Eulamultiple paternityrus heatwolei. Mol Ecol 11:535–545
Olsson M, Schwartz TS, Wapstra E, Shine R (2019) How accurately do behavioral observations predict reproductive success in free-ranging lizards? Biol Lett 15:20190030
Pryke SR (2013) Bird contests: from hatching to fertilisation. In: Hardy IWC, Briffa M (eds) Animal contests. Cambridge University Press, Cambridge, pp 287–303
Rosenthal GG, Stuart-Fox D (2012) Environmental disturbance and animal communication. In: Candolin U, Wong BBM (eds) Behavioral responses to a changing world. Oxford University Press, Oxford, pp 16–31
Salvador A, Díaz JA, Viega JP, Bloor P, Brown RP (2007) Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav Ecol 19:169–176
Stow AJ, Sunnocks P (2004) High mate and site fidelity in Cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol Ecol 13:419–430
Telemeco RS, Baird TA (2011) Capital energy drives production of multiple clutches whereas income energy fuels growth in female collared lizards Crotaphytus collaris. Oikos 120:915–921
Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580
Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Whiting MJ, Nagy KA, Bateman PW (2003) Evaluation and maintenance of social status signalling badges. In: Fox SF, McCoy JK, Baird TA (eds). Johns Hopkins University Press, Baltimore, pp 47–82
Whiting MJ, Miles DB (2019) Behavioral ecology and aggression in lizards. In: Bels VL, Russell AP (eds) Behavior of lizards: evolutionary and mechanistic perspectives. CRC Press, Taylor, pp 289–319
York JR, Baird TA (2015) Testing the adaptive significance of sex-specific mating tactics in collared lizards (Crotaphytus collaris). Biol J Linn Soc 115:423–436
York JR, Baird TA (2017) Sexual selection on male collared lizard (Crotaphytus collaris) display behaviour enhances offspring survivorship. Biol J Linn Soc 122:176–183
York JR, Baird TA (2019) Sexual selection on female collared lizards favours offspring production with multiple males. Anim Behav 147:17–23
Acknowledgements
We thank the U.S. Army Corps of Engineers and the Arcadia Lake Park, Edmond, OK for access to the study site. This research was conducted with the permission of the Oklahoma Department of Wildlife and Institutional and Animal Care and Use Committee at the University of Central Oklahoma to TAB. We thank C.A. Braun, J. Creecy, G. French, M. Haynie, J. Hertzler, S. Hoge, A. Lunsford, A. McGee, C. McGill, C. Moya, D. O’Connor, A. Ruger, Y. Shirali, W. Unsell, and E. York for technical assistance in the field and laboratory, and T.D. Baird for photography.
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We greatly appreciate funding provided by from the Office of Research and Sponsored Programs at the University of Central Oklahoma.
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Troy A. Baird conceived the study, recorded the behavioral data, and collected the blood samples for genetic analyses. Joshua R. York conducted laboratory and genetic analyses, and both authors analyzed the data. TAB wrote the first manuscript draft, both authors made revisions, approved the final manuscript, and provide consent for publication.
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This research was approved by the Institutional Animal Care and Use Committee of the University of Central Oklahoma (IACUC, permit number 13009) and the Oklahoma Department of Wildlife (permit number 5553).
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Baird, T.A., York, J.R. Does courtship behavior predict parentage in Collared Lizards? Influence of male social status and habitat structure. Evol Ecol 35, 795–808 (2021). https://doi.org/10.1007/s10682-021-10136-7
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DOI: https://doi.org/10.1007/s10682-021-10136-7


