Characterisation and cross-amplification of sex-specific genetic markers in Australasian Egerniinae lizards and their implications for understanding the evolution of sex determination and social complexity
Alix Bouffet-Halle A , Weizhao Yang B , Michael G. Gardner C D , Martin J. Whiting E , Erik Wapstra
A , Tobias Uller B and Geoffrey M. While A *
+ Author Affiliations
- Author Affiliations
A School of Natural Sciences, University of Tasmania, Hobart, Tas. 7005, Australia.
B Department of Biology, Lund University, Lund, Sweden.
C College of Science and Engineering, Flinders University, Adelaide, SA 5042, Australia.
D Evolutionary Biology Unit, South Australian Museum, Adelaide, SA 5001, Australia.
E Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.
Australian Journal of Zoology 69(2) 33-40 https://doi.org/10.1071/ZO21023
Submitted: 11 June 2021 Accepted: 29 November 2021 Published: 3 February 2022
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Sex is a pervasive factor that underpins functional phenotypic variation across a range of traits. Although sex can usually be distinguished morphologically, in some species this is not possible. The development of genetic markers for sex identification is, thus, key if we are to incorporate sex into an understanding of ecological or evolutionary process. Here we develop genetic markers for the identification of sex within an iconic Australian lizard group, the Egernia group, which is notable for its complex social behaviour. We used restriction-site associated DNA sequencing to characterise sex-specific genetic sequences for a key member of the group, Liopholis whitii, and designed primers for four of these putative sex-specific sequences. These primers amplified across some, but not all, species of the group. Our results provided several important insights. They suggest conservatism of a XX/XY sex determination system within the group as well as sex-specific genomic regions that appear independent of the conserved genomic regions identified in other skink species. More broadly, the development of sex markers for the Egernia group opens up a range of potential research questions related to the role that sex plays in the mediation of social behaviour and, through this, the emergence and stability of social life.
Keywords: Egernia, Liopholis, RAD-Seq, reptiles, sex chromosomes, sex determination, sex marker, social behaviour.
References
Alam, SMI, Altmanová, M, Prasongmaneerut, T, Georges, A, Sarre, SD, Nielsen, SV, Gamble, T, Srikulnath, K, Rovatsos, M, Kratochvíl, L, and Ezaz, T (2020). Cross-species BAC mapping highlights conservation of chromosome synteny across dragon lizards (Squamata: Agamidae). Genes 11, 698.| Cross-species BAC mapping highlights conservation of chromosome synteny across dragon lizards (Squamata: Agamidae).Crossref | GoogleScholarGoogle Scholar |
Alföldi, J, Di Palma, F, Grabherr, M, Williams, C, Kong, L, Mauceli, E, Russell, P, Lowe, CB, Glor, RE, Jaffe, JD, Ray, DA, Boissinot, S, Shedlock, AM, Botka, C, Castoe, TA, Colbourne, JK, Fujita, MK, Moreno, RG, ten Hallers, BF, Haussler, D, Heger, A, Heiman, D, Janes, DE, Johnson, J, de Jong, PJ, Koriabine, MY, Lara, M, Novick, PA, Organ, CL, Peach, SE, Poe, S, Pollock, DD, de Queiroz, K, Sanger, T, Searle, S, Smith, JD, Smith, Z, Swofford, R, Turner-Maier, J, Wade, J, Young, S, Zadissa, A, Edwards, SV, Glenn, TC, Schneider, CJ, Losos, JB, Lander, ES, Breen, M, Ponting, CP, and Lindblad-Toh, K (2011). The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477, 587–591.
| The genome of the green anole lizard and a comparative analysis with birds and mammals.Crossref | GoogleScholarGoogle Scholar | 21881562PubMed |
Alonso, JC, Martín, E, Morales, MB, and Alonso, JA (2018). Sibling competition and not maternal allocation drives differential offspring feeding in a sexually size-dimorphic bird. Animal Behaviour 137, 35–44.
| Sibling competition and not maternal allocation drives differential offspring feeding in a sexually size-dimorphic bird.Crossref | GoogleScholarGoogle Scholar |
Andrade, P, Pinho, C, de Lanuza, GPI, Afonso, S, Brejcha, J, Rubin, C-J, Wallerman, O, Pereira, P, Sabatino, SJ, Bellati, A, Pellitteri-Rosa, D, Bosakova, Z, Bunikis, I, Carretero, MA, Feiner, N, Marsik, P, Paupério, F, Salvi, D, Soler, L, While, GM, Uller, T, Font, E, Andersson, L, and Carneiro, M (2019). Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard. Proceedings of the National Academy of Sciences of the United States of America 116, 5633–5642.
| Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard.Crossref | GoogleScholarGoogle Scholar | 30819892PubMed |
Arnold, KE, and Griffiths, R (2003). Sex-specific hatching order, growth rates and fledging success in jackdaws Corvus monedula. Journal of Avian Biology 34, 275–281.
| Sex-specific hatching order, growth rates and fledging success in jackdaws Corvus monedula.Crossref | GoogleScholarGoogle Scholar |
Bachtrog, D, Mank, JE, Peichel, CL, Kirkpatrick, M, Otto, SP, Ashman, T, Hahn, MW, Kitano, J, Mayrose, I, Ming, R, Perrin, N, Ross, L, Valenzua, N, and Vamosi, JC Bachtrog, D, Mank, JE, Peichel, CL, Kirkpatrick, M, Otto, SP, Ashman, T, Hahn, MW, Kitano, J, Mayrose, I, Ming, R, Perrin, N, Ross, L, Valenzua, N, and Vamosi, JC (2014). Sex determination: why so many ways of doing it? PLoS Biology 12, e1001899.
| Sex determination: why so many ways of doing it?Crossref | GoogleScholarGoogle Scholar | 24983465PubMed |
Badyaev, AV, Hill, GE, Beck, ML, Dervan, AA, Duckworth, RA, McGraw, KJ, Nolan, PM, and Whittingham, LA (2002). Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295, 316–318.
| Sex-biased hatching order and adaptive population divergence in a passerine bird.Crossref | GoogleScholarGoogle Scholar | 11786641PubMed |
Bels VL, Russel AP (2019) ‘Behavior of Lizards.’ (CRC Press: New Hampshire)
Blackburn, DG (2006). Squamate reptiles as model organisms for the evolution of viviparity. Herpetological Monographs 20, 131–146.
| Squamate reptiles as model organisms for the evolution of viviparity.Crossref | GoogleScholarGoogle Scholar |
Böhme, W (1995). Hemiclitoris discovered: a fully differentiated erectile structure in female monitor lizards (Varanus spp.) (Reptilia: Varanidae). Journal of Zoological Systematics and Evolutionary Research 33, 129–132.
| Hemiclitoris discovered: a fully differentiated erectile structure in female monitor lizards (Varanus spp.) (Reptilia: Varanidae).Crossref | GoogleScholarGoogle Scholar |
Bonisoli-Alquati, A, Boncoraglio, G, Caprioli, M, and Saino, N (2011). Birth order, individual sex and sex of competitors determine the outcome of conflict among siblings over parental care. Proceedings of the Royal Society B: Biological Sciences 278, 1273–1279.
| Birth order, individual sex and sex of competitors determine the outcome of conflict among siblings over parental care.Crossref | GoogleScholarGoogle Scholar | 20943688PubMed |
Catchen, JM, Amores, A, Hohenlohe, P, Cresko, W, and Postlethwait, JH (2011). Stacks: building and genotyping loci de novo from short-read sequences. G3: Genes, Genomes, Genetics 1, 171–182.
| Stacks: building and genotyping loci de novo from short-read sequences.Crossref | GoogleScholarGoogle Scholar |
Chapple, DG (2003). Ecology, life-history, and behavior in the Australian scincid genus Egernia, with comments on the evolution of complex sociality in lizards. Herpetological Monographs 17, 145–180.
| Ecology, life-history, and behavior in the Australian scincid genus Egernia, with comments on the evolution of complex sociality in lizards.Crossref | GoogleScholarGoogle Scholar |
Chapple, DG (2005). Life history and reproductive ecology of White’s skink, Egernia whitii. Australian Journal of Zoology 53, 353–360.
| Life history and reproductive ecology of White’s skink, Egernia whitii.Crossref | GoogleScholarGoogle Scholar |
Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) ‘Dispersal.’ (Oxford University Press: Oxford)
Cooper, SJB, Bull, CM, and Gardner, MG (1997). Characterization of microsatellite loci from the socially monogamous lizard Tiliqua rugosa using a PCR-based isolation technique. Molecular Ecology 6, 793–795.
| Characterization of microsatellite loci from the socially monogamous lizard Tiliqua rugosa using a PCR-based isolation technique.Crossref | GoogleScholarGoogle Scholar |
Cornejo-Páramo, P, Dissanayake, DSB, Lira-Noriega, A, Martínez-Pacheco, ML, Acosta, A, Ramírez-Suástegui, C, Méndez-de-la-Cruz, FR, Székely, T, Urrutia, AO, Georges, A, and Cortez, D (2020). Viviparous reptile regarded to have temperature-dependent sex determination has old XY chromosomes. Genome Biology and Evolution 12, 924–930.
| Viviparous reptile regarded to have temperature-dependent sex determination has old XY chromosomes.Crossref | GoogleScholarGoogle Scholar | 32433751PubMed |
Donnellan SC (1985) The evolution of sex chromosomes in scincid lizards. PhD Thesis, Macquarie University, Sydney, NSW, Australia.
Donnellan, SC (1991). Chromosomes of Australian lygosomine skinks (Lacertilia: Scincidae). Genetica 83, 207–222.
| Chromosomes of Australian lygosomine skinks (Lacertilia: Scincidae).Crossref | GoogleScholarGoogle Scholar |
Ellegren, H, and Sheldon, BC (1997). New tools for sex identification and the study of sex allocation in birds. Trends in Ecology & Evolution 12, 255–259.
| New tools for sex identification and the study of sex allocation in birds.Crossref | GoogleScholarGoogle Scholar |
Ezaz, T, Quinn, AE, Sarre, SD, O’Meally, D, Georges, A, and Marshall Graves, JA (2009a). Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards. Chromosome Research 17, 91–98.
| Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards.Crossref | GoogleScholarGoogle Scholar | 19172405PubMed |
Ezaz, T, Sarre, SD, O’Meally, D, Marshall Graves, JA, and Georges, A (2009b). Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenetic and Genome Research 127, 249–260.
| Sex chromosome evolution in lizards: independent origins and rapid transitions.Crossref | GoogleScholarGoogle Scholar | 20332599PubMed |
Fernando, P, and Melnick, DJ (2001). Molecular sexing eutherian mammals. Molecular Ecology Notes 1, 350–353.
| Molecular sexing eutherian mammals.Crossref | GoogleScholarGoogle Scholar |
Frank, LG, Glickman, SE, and Licht, P (1991). Fatal sibling aggression, precocial development, and androgens in neonatal spotted hyenas. Science 252, 702–704.
| Fatal sibling aggression, precocial development, and androgens in neonatal spotted hyenas.Crossref | GoogleScholarGoogle Scholar | 2024122PubMed |
Gamble, T (2010). A review of sex determining mechanisms in geckos (Gekkota: Squamata). Sexual Development 4, 88–103.
| A review of sex determining mechanisms in geckos (Gekkota: Squamata).Crossref | GoogleScholarGoogle Scholar | 20234154PubMed |
Gamble, T, Coryell, J, Ezaz, T, Lynch, J, Scantlebury, DP, and Zarkower, D (2015). Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Molecular Biology and Evolution 32, 1296–1309.
| Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems.Crossref | GoogleScholarGoogle Scholar | 25657328PubMed |
Gardner, MG, Hugall, AF, Donnellan, SC, Hutchinson, MN, and Foster, R (2008). Molecular systematics of social skinks: phylogeny and taxonomy of the Egernia group (Reptilia: Scincidae). Zoological Journal of the Linnean Society 154, 781–794.
| Molecular systematics of social skinks: phylogeny and taxonomy of the Egernia group (Reptilia: Scincidae).Crossref | GoogleScholarGoogle Scholar |
Gardner, MG, Pearson, SK, Johnston, GR, and Schwarz, MP (2016). Group living in squamate reptiles: a review of evidence for stable aggregations. Biological Reviews 91, 925–936.
| Group living in squamate reptiles: a review of evidence for stable aggregations.Crossref | GoogleScholarGoogle Scholar | 26052742PubMed |
Golla, W, Hofer, H, and East, ML (1999). Within-litter sibling aggression in spotted hyaenas: effect of maternal nursing, sex and age. Animal Behaviour 58, 715–726.
| Within-litter sibling aggression in spotted hyaenas: effect of maternal nursing, sex and age.Crossref | GoogleScholarGoogle Scholar | 10512644PubMed |
Griffiths, R, and Tiwari, B (1995). Sex of the last wild Spix’s macaw. Nature 375, 454.
| Sex of the last wild Spix’s macaw.Crossref | GoogleScholarGoogle Scholar | 7777052PubMed |
Griffiths, R, Double, MC, Orr, K, and Dawson, RJG (1998). A DNA test to sex most birds. Molecular Ecology 7, 1071–1075.
| A DNA test to sex most birds.Crossref | GoogleScholarGoogle Scholar | 9711866PubMed |
Halliwell, B, Uller, T, Wapstra, E, and While, GM (2017). Resource distribution mediates social and mating behavior in a family living lizard. Behavioral Ecology 28, 145–153.
| Resource distribution mediates social and mating behavior in a family living lizard.Crossref | GoogleScholarGoogle Scholar |
Hamilton, WD (1967). Extraordinary sex ratios. Science 156, 477–488.
| Extraordinary sex ratios.Crossref | GoogleScholarGoogle Scholar | 6021675PubMed |
Hill, P, Shams, F, Burridge, CP, Wapstra, E, and Ezaz, T (2021). Differences in homomorphic sex chromosomes are associated with population divergence in sex determination in Carinascincus ocellatus (Scincidae: Lygosominae). Cells 10, 291.
| Differences in homomorphic sex chromosomes are associated with population divergence in sex determination in Carinascincus ocellatus (Scincidae: Lygosominae).Crossref | GoogleScholarGoogle Scholar | 33535518PubMed |
Kasperoviczus, KN, dos Santos, LC, and Almeida-Santos, SM (2011). First report of hemiclitores in a female of the amphisbaenian Amphisbaena microcephala (Wagler, 1824). Herpetology Notes 4, 41–43.
Komdeur, J, Daan, S, Tinbergen, J, and Mateman, C (1997). Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs. Nature 385, 522–525.
| Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs.Crossref | GoogleScholarGoogle Scholar |
Komdeur, J, and Pen, I (2002). Adaptive sex allocation in birds: the complexities of linking theory and practice. Philosophical Transactions of the Royal Society B: Biological Sciences 357, 373–380.
| Adaptive sex allocation in birds: the complexities of linking theory and practice.Crossref | GoogleScholarGoogle Scholar |
Koressaar, T, and Remm, M (2007). Enhancements and modifications of primer design program Primer3. Bioinformatics 23, 1289–1291.
| Enhancements and modifications of primer design program Primer3.Crossref | GoogleScholarGoogle Scholar | 17379693PubMed |
Kostmann, A, Kratochvíl, L, and Rovatsos, M (2021). Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation. Proceedings of the Royal Society B: Biological Sciences 288, 20202139.
| Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation.Crossref | GoogleScholarGoogle Scholar | 33468012PubMed |
Lawson Handley, LJ, and Perrin, N (2007). Advances in our understanding of mammalian sex-biased dispersal. Molecular Ecology 16, 1559–1578.
| Advances in our understanding of mammalian sex-biased dispersal.Crossref | GoogleScholarGoogle Scholar | 17402974PubMed |
Literman, R, Radhakrishnan, S, Tamplin, J, Burke, R, Dresser, C, and Valenzuela, N (2017). Development of sexing primers in Glyptemys insculpta and Apalone spinifera turtles uncovers an XX/XY sex-determining system in the critically-endangered bog turtle Glyptemys muhlenbergii. Conservation Genetics Resources 9, 651–658.
| Development of sexing primers in Glyptemys insculpta and Apalone spinifera turtles uncovers an XX/XY sex-determining system in the critically-endangered bog turtle Glyptemys muhlenbergii.Crossref | GoogleScholarGoogle Scholar |
Liu, Y, Zhou, Q, Wang, Y, Luo, L, Yang, J, Yang, L, Liu, M, Li, Y, Qian, T, Zheng, Y, Li, M, Li, J, Gu, Y, Han, Z, Xu, M, Wang, Y, Zhu, C, Yu, B, Yang, Y, Ding, F, Jiang, J, Yang, H, and Gu, X (2015). Gekko japonicus genome reveals evolution of adhesive toe pads and tail regeneration. Nature Communications 6, 10033.
| Gekko japonicus genome reveals evolution of adhesive toe pads and tail regeneration.Crossref | GoogleScholarGoogle Scholar | 26598231PubMed |
Miyaki, CY, Griffiths, R, Orr, K, Nahum, LA, Pereira, SL, and Wajntal, A (1998). Sex identification of parrots, toucans, and curassows by PCR: perspectives for wild and captive population studies. Zoo Biology 17, 415–423.
| Sex identification of parrots, toucans, and curassows by PCR: perspectives for wild and captive population studies.Crossref | GoogleScholarGoogle Scholar |
Peterson, BK, Weber, JN, Kay, EH, Fisher, HS, and Hoekstra, HE (2012). Double digest RADseq: an inexpensive method for denovo SNP discovery and genotyping in model and non-model species. PLoS ONE 7, e37135.
| Double digest RADseq: an inexpensive method for denovo SNP discovery and genotyping in model and non-model species.Crossref | GoogleScholarGoogle Scholar | 22675423PubMed |
Prugnolle, F, and de Meeus, T (2002). Inferring sex-biased dispersal from population genetic tools: a review. Nature 88, 161–165.
| Inferring sex-biased dispersal from population genetic tools: a review.Crossref | GoogleScholarGoogle Scholar |
Pyron, RA, Burbrink, FT, and Wiens, JJ (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology 13, 93.
| A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes.Crossref | GoogleScholarGoogle Scholar | 23627680PubMed |
Rheubert JL, Siegel DS, Trauth SE (2014) ‘Reproductive Biology and Phylogeny of Lizards and Tuatara’, 1st Edn. (CRC Press: Enfield, NH, USA)
Richardson, DS, Burke, T, and Komdeur, J (2002). Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers. Evolution 56, 2313–2321.
| Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers.Crossref | GoogleScholarGoogle Scholar | 12487360PubMed |
Romanov, MN, Betuel, AM, Chemnick, LG, Ryder, OA, Kulibaba, RO, Tereshchenko, OV, Payne, WS, Delekta, PC, Dodgson, JB, Tuttle, EM, and Gonser, RA (2019). Widely applicable PCR markers for sex identification in birds. Russian Journal of Genetics 55, 220–231.
| Widely applicable PCR markers for sex identification in birds.Crossref | GoogleScholarGoogle Scholar |
Rovatsos, M, and Kratochvíl, L (2017). Molecular sexing applicable in 4000 species of lizards and snakes? From dream to real possibility. Methods in Ecology and Evolution 8, 902–906.
| Molecular sexing applicable in 4000 species of lizards and snakes? From dream to real possibility.Crossref | GoogleScholarGoogle Scholar |
Sarre, SD, Ezaz, T, and Georges, A (2011). Transitions between sex-determining systems in reptiles and amphibians. Annual Review of Genomics and Human Genetics 12, 391–406.
| Transitions between sex-determining systems in reptiles and amphibians.Crossref | GoogleScholarGoogle Scholar | 21801024PubMed |
Sigeman, H, Ponnikas, S, and Hansson, B (2020). Whole-genome analysis across 10 songbird families within Sylvioidea reveals a novel autosome–sex chromosome fusion. Biology Letters 16, 20200082.
| Whole-genome analysis across 10 songbird families within Sylvioidea reveals a novel autosome–sex chromosome fusion.Crossref | GoogleScholarGoogle Scholar | 32315592PubMed |
Srikulnath, K, Azad, B, Singchat, W, and Ezaz, T (2019). Distribution and amplification of interstitial telomeric sequences (ITSs) in Australian dragon lizards support frequent chromosome fusions in Iguania. PLoS ONE 14, e0212683.
| Distribution and amplification of interstitial telomeric sequences (ITSs) in Australian dragon lizards support frequent chromosome fusions in Iguania.Crossref | GoogleScholarGoogle Scholar | 30794668PubMed |
Stow, AJ, Sunnucks, P, Briscoe, DA, and Gardner, MG (2001). The impact of fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites. Molecular Ecology 10, 867–878.
| The impact of fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites.Crossref | GoogleScholarGoogle Scholar | 11348496PubMed |
Trochet, A, Stevens, VM, Baguette, M, Chaine, A, Schmeller, DS, and Clobert, J (2016). Evolution of sex-biased dispersal. The Quarterly Review of Biology 91, 297–320.
| Evolution of sex-biased dispersal.Crossref | GoogleScholarGoogle Scholar | 29558614PubMed |
Uetz P, Freed P, Hošek J (2019) The reptile database. Available at http://www.reptile-database.org. [Accessed 23 April 2020]
Uller, T (2006). Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios. Biological Reviews 81, 207–217.
| Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios.Crossref | GoogleScholarGoogle Scholar | 16677432PubMed |
Uller, T, Pen, I, Wapstra, E, Beukeboom, LW, and Komdeur, J (2007). The evolution of sex ratios and sex-determining systems. Trends in Ecology & Evolution 22, 292–297.
| The evolution of sex ratios and sex-determining systems.Crossref | GoogleScholarGoogle Scholar |
Valdecantos, S, and Lobo, F (2015). First report of hemiclitores infemales of South American liolaemid lizards. Journal of Herpetology 49, 291–294.
| First report of hemiclitores infemales of South American liolaemid lizards.Crossref | GoogleScholarGoogle Scholar |
Wapstra, E, Uller, T, Pen, I, Komdeur, J, Olsson, M, and Shine, R (2007). Disentangling the complexities of vertebrate sex allocation: a role for squamate reptiles? Oikos 116, 1051–1057.
| Disentangling the complexities of vertebrate sex allocation: a role for squamate reptiles?Crossref | GoogleScholarGoogle Scholar |
Warner, DA, Du, W-G, and Georges, A (2018). Introduction to the special issue – developmental plasticity in reptiles: physiological mechanisms and ecological consequences. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 329, 153–161.
| Introduction to the special issue – developmental plasticity in reptiles: physiological mechanisms and ecological consequences.Crossref | GoogleScholarGoogle Scholar |
While, GM, Jones, SM, and Wapstra, E (2007). Birthing asynchrony is not a consequence of asynchronous offspring development in a non-avian vertebrate, the Australian skink Egernia whitii. Functional Ecology 21, 513–519.
| Birthing asynchrony is not a consequence of asynchronous offspring development in a non-avian vertebrate, the Australian skink Egernia whitii.Crossref | GoogleScholarGoogle Scholar |
While, GM, Uller, T, and Wapstra, E (2011). Variation in social organization influences the opportunity for sexual selection in a social lizard. Molecular Ecology 20, 844–852.
| Variation in social organization influences the opportunity for sexual selection in a social lizard.Crossref | GoogleScholarGoogle Scholar | 21199033PubMed |
While, GM, Uller, T, Bordogna, G, and Wapstra, E (2014). Promiscuity resolves constraints on social mate choice imposed by population viscosity. Molecular Ecology 23, 721–732.
| Promiscuity resolves constraints on social mate choice imposed by population viscosity.Crossref | GoogleScholarGoogle Scholar | 24354676PubMed |
While GM, Gardner MG, Chapple DG, Whiting MJ (2019) Stable social grouping in lizards. In ‘Behavior of Lizards’. (Eds A Russel, V Bells) pp. 321–339. (CRC Press: Enfield, NH, USA)
Whiting MJ, While GM (2017) Sociality in lizards. In ‘Comparative Social Evolution’. (Eds D Rubenstein, P Abbot) pp. 390–426. (Cambridge University Press: Cambridge, UK)
Wilson EO (1975) ‘Sociobiology: the New Synthesis.’ (Harvard University Press: Cambridge, MA, USA)
