Environmental constraints and genetic basis for the evolution of viviparity

Recknagel, Hans (2018) Environmental constraints and genetic basis for the evolution of viviparity. PhD thesis, University of Glasgow.

Abstract

The evolution of live-bearing (viviparity) from egg-laying (oviparity) is one of the most complex life history transitions in the animal kingdom. Yet, it has repeatedly and independently evolved across various animal groups, ranging across almost all major groups including invertebrates, fishes, amphibians, reptiles and mammals. In squamate reptiles, this transition has occurred about 100 times independently, more frequently than in any other vertebrate group. Why do transitions to viviparity occur? The evolutionary drivers for these transitions are not fully understood. Associated life-history advantages and disadvantages between parity modes are manifold, and might vary from case to case, but are difficult to compare in a controlled environment while minimizing phylogenetic effects. Transitions usually occur only into one direction, from an oviparous ancestor to a viviparous descendant. The eggshell is a complex feature, and once lost – according to Dollo’s law of irreversibility – thought to be impossible to be regained. However, in squamates some cases have been discussed controversially that potentially re-evolved oviparity. Finally, in addition to understanding why transitions occur, we know very little about how transitions occur. Given that most transitions occurred in the deep evolutionary past, it is difficult to infer the genetic mechanism of how such complex traits originate. To understand how major evolutionary innovations and complex traits arise, it is indispensable to understand their genetic underpinnings.

Cold climate has been suggested to be the causal driver for transitions to viviparity. Egg clutch survival depends on the external environment, and if the environment is too cool, consequences are retarded embryonic development or even lethal freezing. Viviparous females have more control on the survival of their offspring by choosing the optimal temperature for embryonic development. The proportion of viviparous species increases with latitude, but whether viviparity evolved as a result of cooler temperatures in the first place is still unknown. I used molecular dating methods to infer at which time points transitions to viviparity occurred across the squamate tree and linked this to paleoclimatic data from the last 65 million years. I found that transitions generally occurred during cold and stable climatic conditions. This supports the prediction from the cold-climate hypothesis, but also shows for the first time that a stable environment is important for this evolutionary transition, linking life-history and cold-climate predictions.

The possibility of back-transitions from a viviparous ancestor to an oviparous descendant in squamate reptiles has been discussed rigorously. The re-evolution of a complex trait (such as the eggshell) is evolutionarily very unlikely, according to Dollo’s law even impossible. However, a few exceptions in nature are known, such as the re-evolution of wings in stick insects or the re-evolution of sexuality in mites. Within common lizards, two lineages are egg-laying and four lineages are live-bearing. Earlier phylogenetic work suggested several hypotheses for parity mode evolution, including a single transition to viviparity, multiple transitions to viviparity and a reversal to oviparity. Using genome-wide SNP genotyping, I reconstructed the evolutionary history of parity modes and found that a single origin of viviparity and a reversal to oviparity was the most parsimonious phylogenetic scenario. The phylogeny was consistent with chromosomal data and supported as significantly more likely than alternative scenarios by topology testing and ancestral trait reconstructions. I suggest that common lizards represent a rare case of a reversal to oviparity, breaking Dollo’s law of irreversibility.

The transition from oviparity to viviparity is complex, and comes with several changes in morphology, physiology and behaviour. Several life-history trade-offs between the two parity modes have been suggested, but analyses often suffer from confounding environmental and/or phylogenetic effects. It is predicted that viviparous species are larger in body size, produce less, but larger offspring with enhanced survival, and exhibit a larger reproductive burden. I tested if life-history traits in reproductively bimodal oviparous and viviparous common lizard (Zootoca vivipara) differed. I preformed this in a unique natural setting, a contact zone between both reproductive modes. The model system is almost ideal to study trade-offs between reproductive modes, as the transition is evolutionarily very young and the two parity modes occur in the same environment. I found that viviparous females have larger body sizes, smaller clutch size but higher offspring survival, and a higher reproductive burden. Contrary to predictions, offspring size and weight was smaller for viviparous females. This might indicate that viviparous common lizards are constrained for womb space. Almost all reproductive traits were significantly associated with body length in viviparous females, but not in oviparous females, suggesting a major impact of body size on reproduction in viviparous females. In general, I suggest that the link between reproductive life-history traits and reproductive mode is context dependent.

Identifying the genetic basis of complex evolutionary transitions is a major goal for evolutionary biologists. This will ultimately help us to understand how the biodiversity we observe today has been generated. However, most complex transitions occurred millions of years ago, making it difficult to discern causal genetic variants from accumulated genomic background noise. An approach to overcome this issue is admixture mapping, which makes use of the natural hybridization of lineages with different fixed phenotypes. Hybridization results in recombination of genetic variants and the disassociation of background noise from the causal genetic variation controlling a phenotype. In a unique hybrid zone between viviparous and oviparous common lizards, I detected loci associated with parity mode. I identified a few genomic regions associated with the trait, including two regions on the sex chromosome and the gene EPAS1 on chromosome 3. A few SNPs were located next to immune response genes, possibly indicating modified immune interactions between mother and embryo in viviparous common lizards. Genome scans across all lineages supported that the sex chromosome is an important region for parity model control. Preliminary analyses suggested that more variants than expected are shared between the two oviparous lineages. However, whether the lineage with derived oviparity uses the same genetic mechanism as the lineage with basal oviparity remains to be investigated in more detail. For the first time, I identified the genetic basis of viviparity and fond it to be controlled by few genes of large effect.

• Item Type: Thesis (PhD)
• Qualification Level: Doctoral
• Additional Information: This project was funded by the Lord Kelvin Adam Smith Scholarship and a Heredity fieldwork grant.
• Subjects: Q Science > QH Natural history; Q Science > QH Natural history > QH301 Biology; Q Science > QL Zoology
• Colleges/Schools: College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
• Supervisor's Name: Elmer, Dr. Kathryn and Kamenos, Dr. Nick
• Date of Award: 2018
• Embargo Date: 12 July 2022
• Depositing User: Mrs Marie Cairney
• Unique ID: glathesis:2018-30688
• Copyright: Copyright of this thesis is held by the author.
• Date Deposited: 12 Jul 2018 09:56
• Last Modified: 16 Oct 2024 09:08
• Thesis DOI: 10.5525/gla.thesis.30688
• URI: https://theses.gla.ac.uk/id/eprint/30688

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