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The functional genetic architecture of egg-laying and live-bearing reproduction in common lizards

Nature Ecology & Evolution volume 5, pages 1546–1556 (2021)Cite this article

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Abstract

All amniotes reproduce either by egg-laying (oviparity), which is ancestral to vertebrates or by live-bearing (viviparity), which has evolved many times independently. However, the genetic basis of these parity modes has never been resolved and, consequently, its convergence across evolutionary scales is currently unknown. Here, we leveraged natural hybridizations between oviparous and viviparous common lizards (Zootoca vivipara) to describe the functional genes and genetic architecture of parity mode and its key traits, eggshell and gestation length, and compared our findings across vertebrates. In these lizards, parity trait genes were associated with progesterone-binding functions and enriched for tissue remodelling and immune system pathways. Viviparity involved more genes and complex gene networks than did oviparity. Angiogenesis, vascular endothelial growth and adrenoreceptor pathways were enriched in the viviparous female reproductive tissue, while pathways for transforming growth factor were enriched in the oviparous. Natural selection on these parity mode genes was evident genome-wide. Our comparison to seven independent origins of viviparity in mammals, squamates and fish showed that genes active in pregnancy were related to immunity, tissue remodelling and blood vessel generation. Therefore, our results suggest that pre-established regulatory networks are repeatedly recruited for viviparity and that these are shared at deep evolutionary scales.

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Fig. 1: Natural hybridization and backcrossing between oviparous and viviparous common lizards result in intermediate phenotypes and genotypes.
Fig. 2: Genetic architecture of parity mode.
Fig. 3: Differential expression analyses between oviparous and viviparous uterine tissue during pregnancy.
Fig. 4: Genome-wide analysis of selection score (-log10P from PCAdapt) versus genetic differentiation (FST) between adult common lizards spanning oviparity to viviparity (64,846 loci).
Fig. 5: Overlap between differentially expressed genes in pregnant and non-pregnant viviparous vertebrates.

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Data availability

The raw sequence data presented in this paper can be found on NCBI (NCBI BioProject ID PRJNA657575; https://www.ncbi.nlm.nih.gov/bioproject/PRJNA657575/). The genotype file and list of DEGs can be found at the University of Glasgow Enlighten repository (https://doi.org/10.5525/gla.researchdata.1138)75.

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Acknowledgements

We thank the late W. Mayer for his support and guidance in developing the project. For technical assistance, we are grateful to A. Adams, M. Capstick, M. Mullin and J. Galbraith. We thank K. Schneider for assistance with whole-genome resequencing libraries. We thank H. Leitao, T. Caribe da Rocha, M. Mullin and J. Gallagher for help with eggshell sample preparation and calcium content measurements. We thank R. Page for support in project development, A. Jacobs for discussions and comments on data analysis and T. Stevenson for comments on a draft. We thank G. Migiani for creating some illustrations used in the figures. Finally, many thanks are due to the field assistants M. Andrews, M. Capstick, R. Carey, K. Gallagher-Mackay, M. Lamorgese, N. Lawrie, M. Layton, H. Leitão, J. McClelland, G. Migiani, M. Raske, J. Smout and M. Sutherland who helped with sampling and husbandry. Sampling permission was issued by local authorities under multiyear permit no. HE3-NS-959/2013. Research was funded by: a Genetics Society Heredity Fieldwork grant to H.R.; a University of Glasgow Lord Kelvin/Adam Smith PhD studentship to K.R.E., N.A.K. and H.R.; and NERC grants NE/ N003942/1 to K.R.E. and M.M.B. with R.D.M. Page, NBAF964 to K.R.E. and NBAF1018 to K.R.E. and A.Y.

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Author notes

  1. Hans Recknagel

    Present address: Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

  2. Madeleine Carruthers

    Present address: School of Biological Sciences, University of Bristol, Bristol, UK

  3. Andrey A. Yurchenko

    Present address: Inserm U981, Gustave Roussy Cancer Campus, Université Paris Saclay, Villejuif, France

Authors and Affiliations

  1. Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK

    Hans Recknagel, Madeleine Carruthers, Andrey A. Yurchenko, Mohsen Nokhbatolfoghahai, Maureen M. Bain & Kathryn R. Elmer

  2. School of Geographical and Earth Sciences, University of Glasgow, Glasgow, UK

    Nicholas A. Kamenos

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Contributions

H.R., M.M.B., N.A.K. and K.R.E. designed and led the project. H.R. and K.R.E carried out the fieldwork. H.R. conducted the phenotypic analyses, generated and analysed the genomic data and genetic mapping, generated and interpreted the transcriptome data, and compiled and analysed the comparative analyses. M.N. staged the embryonic development. M.C. conducted transcriptome bioinformatics. A.Y. assembled and annotated the reference genome and conducted whole-genome bioinformatics. H.R. and M.M.B. conducted the eggshell microscopy. H.R. and M.C. produced the figures. H.R. and K.R.E. wrote the manuscript with contributions from M.C. and A.Y. All authors contributed to interpreting the results and revising the manuscript.

Corresponding author

Correspondence to Kathryn R. Elmer.

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The authors declare no competing interests.

Additional information

Peer review information Nature Ecology & Evolution thanks Gunter Wagner and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Distribution of common lizards in Europe.

a, The distribution of oviparous (dark brown) and viviparous (light brown) common lizard lineages. b, The sampling area for this study, a contact zone in Austria with overlapping oviparous and viviparous common lizards, including hybrids (Q-value 0.1–0.9). The map was drawn in R using Google Map data retrieved by API Key.

Extended Data Fig. 2 Histograms of all reproductive phenotypes describing parity mode characteristics.

a, The number of external incubation days was measured for each clutch in the field, and b, one sample per clutch was taken to identify the embryonic stage at oviposition/parturition. c, From these two phenotypes, a gestation time score was calculated, where 0 is more viviparous and 1 is more oviparous. To describe eggshell characteristics, d, calcium content and e, eggshell thickness were measured for one eggshell per clutch. f, From these two phenotypes, an eggshell score was calculated for each individual, where 0 is more viviparous and 1 is more oviparous.

Extended Data Fig. 3 Correlation between reproductive phenotypes and genome-wide ancestry.

Correlations between reproductive traits and summary scores for a–c, gestation time and d–f, eggshell characteristics are shown plotted against genome-wide Q-value for parity mode (0 = oviparous, 1 = viviparous) inferred from ADMIXTURE.

Extended Data Fig. 4

Decay of linkage disequilibrium (LD) in candidate regions for chromosomes containing SNPs significantly associated with parity mode.

Extended Data Fig. 5 Genetic associations between reproductive phenotypes and 80,696 SNPs.

Manhattan plots from admixture mapping analyses on the four individually measured reproductive traits: a, incubation days, b, embryonic stage, c, calcium content, d, eggshell thickness. The genome-wide significance is indicated by the horizontal red dotted line, while the blue line indicates a p-value threshold of <0.01 using the Benjamini–Hochberg correction.

Extended Data Fig. 6 RNA expression across 14,102 genes for oviparous and viviparous females at different reproductive stages in multi-dimensional space.

a, Schematic timeline of the reproductive season of oviparous and viviparous common lizards at the sampling location. Sampling times for RNA at early, mid and after parition are indicated with stars. Sampling times reflect embryonic developmental stages (early: < stage 22; mid: stage 23–30). b, A principal component analysis (PCA), and c, a redundancy analysis (RDA) from the RNAseq analysis. d, shows a Venn diagram of the overlap of differential gene expression between the three stages ‘early’ in pregnancy, ‘mid’ pregnancy and ‘after’ pregnancy. Genes that were differentially expressed (DE) either during ‘early’, ‘mid’ or both ‘early’ and ‘mid’ were considered as functionally important DE genes (noted with asterisks), excluding those that also overlapped ‘after’ pregnancy.

Extended Data Fig. 7 Genome-wide selection scan and estimates of diversity and divergence.

a, Out of a total of 80,696 SNPs, those highlighted in blue and red (N = 1051 SNPs) showed significant signals of selection (Benjamini–Hochberg corrected p-value < 0.01). In addition, all SNPs in red (N = 128 SNPs) are those associated with reproductive traits via admixture mapping analyses. Nucleotide diversity estimates within b, oviparous and c, viviparous common lizards. Smoothed means are shown in dark brown for oviparous and light brown for viviparous. d, shows FST across the genome. Candidate regions are marked as red bars. Standard deviations of smoothed means are shown in light grey. e, Genome-wide difference in coverage between a male and female common lizard, suggesting regions on chromosome 7 and 8 act as sex chromosomes where coverage in the female/heterogametic sex is lower.

Extended Data Fig. 8 Correlation between selection scores (shown as negative Log10 P) and genetic differentiation and diversity measures.

SNP selection scores positively correlate with a, FST and with b, overall nucleotide diversity when all individuals are pooled. Within both c, oviparous and d, viviparous parity modes, nucleotide diversity negatively correlates with selection scores.

Extended Data Fig. 9 Comparative assessment of functional genes.

a, Overlap in differentially expressed genes between viviparous mammals during pregnancy. Species comparisons in each histogram are shown in turquoise circles. A phylogenetic tree of the included viviparous mammals shows estimated divergence times. Note that all species diverged from a common egg-laying ancestor around 160 million years ago. ***P < 0.001. Divergence times were derived from TimeTree42. b, Correlation between unfiltered gene lists extracted from literature and gene lists filtered with the Database for Annotation, Visualization and Integrated Discovery (DAVID). Gene lists filtered with DAVID were based on human and chicken gene symbols. While some genes (on average 6.9%) are lost using the filtering, the fold enrichment of observed versus expected overlap of gene lists between all possible intersections across viviparous vertebrates was highly correlated (R2 = 0.997).

Extended Data Fig. 10 Correlation between reproductive phenotypes.

Correlations between all reproductive phenotypes from females: combinations of embryonic stage at parition, number of external incubation days from parition to hatching, eggshell thickness, and calcium content in eggshells.

Supplementary information

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Supplementary Methods, Tables 1–17 and references.

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Recknagel, H., Carruthers, M., Yurchenko, A.A. et al. The functional genetic architecture of egg-laying and live-bearing reproduction in common lizards. Nat Ecol Evol 5, 1546–1556 (2021). https://doi.org/10.1038/s41559-021-01555-4

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