D4- The macroevolution and macroecology of reproductive mode

A global analysis of viviparity in squamates highlights its prevalence in cold climates, Anna Zimin et al., 2022

• Aim→ Viviparity has evolved more times in squamates than in any other vertebrate group; therefore, squamates offer an excellent model system in which to study the patterns, drivers and implications of reproductive mode evolution. Based on current species distributions, we examined three selective forces hypothesized to drive the evolution of squamate viviparity (cold climate, variable climate and hypoxic conditions) and tested whether viviparity is associated with larger body size.

• Location→ Global

• Time period→ Present day

• Taxon→ Squamata

• Methods→ We compiled a dataset of 9061 squamate species, including their distributions, elevation, climate, body mass and reproductive modes. We applied species-level and assemblage-level approaches for predicting reproductive mode, both globally and within biogeographical realms. We tested the relationships of temperature, interannual and intra-annual climatic variation, elevation (as a proxy for hypoxic conditions) and body mass with reproductive mode, using path analyses to account for correlations among the environmental predictors.

• Results→ Viviparity was strongly associated with cold climates at both species and assemblage levels, despite the prevalence of viviparity in some warm climates. Viviparity was not clearly correlated with climatic variability or elevation. The probability of being viviparous exhibited a weak positive correlation with body size.

• Conclusions→ Although phylogenetic history is important, potentially explaining the occurrence of viviparous species in regions that are warm at present, current global squamate distribution is characterized by a higher relative abundance of viviparity in cold environments, supporting the prediction of the “cold-climate” hypothesis. The roles of climatic variation and hypoxia are less important and not straightforward. Elevation probably exerts various selective pressures and influences the prevalence of viviparity primarily through its effect on temperature rather than on oxygen concentration.

• Viviparity was strongly associated with cold climates at both species and assemblage levels

• Most species in the coldest temperature ranges are viviparous

• The proportion of viviparous species generally increased with absolute latitude

• The richness of oviparous species declines much more rapidly towards lower temperatures than that of viviparous taxa, suggesting stronger selection against oviparity in cold conditions

+ very large dataset from around the world

The "cold-climate" hypothesis is an evolutionary ecology theory that proposes that viviparity (live birth) is selected for in cold regions because the retention of embryos within the mother's body provides a more favourable thermal environment for their development compared to externally laid eggs

• Thermal Advantage: The core of the hypothesis is that by retaining the embryos, the viviparous mother can behaviourally thermoregulate, such as by basking, to maintain a more stable and often warmer body temperature than the surrounding environment . This provides the developing embryos with protection from the deleterious effects of low ambient temperatures.

• Vulnerability of Eggs in Cold Climates: The hypothesis stems from the understanding that oviparous reptiles in cold climates face significant challenges for their developing eggs

• Lack of Insulation: Reptilian eggs typically have poor thermal insulation, making them susceptible to temperature fluctuations, particularly cold temperatures

• Limited Nesting Sites: Cold environments may have a scarcity of protected nesting sites that can buffer eggs from low temperatures, leaving them vulnerable

• Risk of Hypothermia: The combination of lack of insulation and potential exposure to cold can lead to prolonged embryonic development and an increased risk of mortality due to hypothermia

• Benefits of Uterine Retention: Viviparity offers several advantages in overcoming these challenges

• Thermal Buffering: The mother's body acts as a buffer, providing a more stable and often warmer thermal environment for the embryos than they would experience externally

• Controlled Development: Viviparity allows the mother to potentially control the timing of development and offspring release, ensuring they emerge at a more favourable time of the year, even in regions with short warm seasons

• Reduced Predation Risk (Indirect): While eggs are vulnerable to predation for an extended period of development, the period of external vulnerability is eliminated in viviparous species

As we discussed previously, this thermal advantage of viviparity in cold climates may be diminished by the ongoing impacts of global warming, potentially altering the selective pressures on reproductive modes in these regions in the future

Viviparity stimulates diversification in an order of fish, Andrew Helmstetter et al., 2016

• Species richness is distributed unevenly across the tree of life and this may be influenced by the evolution of novel phenotypes that promote diversification.

• Viviparity has originated ∼150 times in vertebrates and is considered to be an adaptation to highly variable environments. Likewise, possessing an annual life cycle is common in plants and insects, where it enables the colonization of seasonal environments, but rare in vertebrates. The extent to which these reproductive life-history traits have enhanced diversification and their relative importance in the process remains unknown.

• We show that convergent evolution of viviparity causes bursts of diversification in fish.

• We built a phylogenetic tree for Cyprinodontiformes, an order in which both annualism and viviparity have arisen, and reveal that while both traits have evolved multiple times, only viviparity played a major role in shaping the patterns of diversity.

• These results demonstrate that changes in reproductive life-history strategy can stimulate diversification.

- is only 1200/35,000 fish species

• annualism→ one generation per year, hibernate in dry season, re-emerge in wet season→ 25% of these

• 27% are viviparous

• models are known to incorrectly estimate low extinction rates

What are the potential trade-offs or disadvantages of viviparity compared to oviparity, and how might these affect species’ survival in different environments?

• Physical Burden on pregnant Females: e.g. impeding movement speed and agility- more vulnerable to predation.

• Reduced Reproductive Rate: Viviparity restricts the female's ability to reproduce again for the duration of pregnancy, leading to a significantly lower rate of reproduction compared to oviparity- days to weeks depending on species

• Increased Cost of Predation: Predation on a gravid viviparous female results in the loss of both the mother and her entire brood, whereas predation on an oviparous female usually does not lead to the loss of her entire clutch of eggs

If viviparity offers such a strong selective advantage in cold climates, how might the ongoing impacts of global warming influence the prevalence or evolution of viviparous species in the future?

• the primary selective advantage of viviparity in cold climates, as supported by the "cold-climate" hypothesis, is the uterine retention of embryos which shields them from the deleterious effects of low temperatures compared to exposed eggs→ As global warming leads to increasing average temperatures and potentially reduced frequency and severity of cold spells, this key advantage of viviparity in these environments might diminish.

• Reduced Selective Pressure for Viviparity: In formerly cold regions that experience significant warming, the selective pressure favouring viviparity over oviparity might weaken. Oviparous species might find it easier for their eggs to develop successfully in warmer conditions, potentially reducing the relative fitness advantage of viviparous species in those areas

• Increased Significance of Viviparity's Costs: As the thermal advantage of viviparity decreases, the inherent trade-offs and disadvantages associated with it, which we discussed previously, might become more prominent. In warmer conditions, these costs might outweigh the diminishing benefits of viviparity, potentially putting viviparous species at a disadvantage compared to oviparous ones that do not face these maternal burdens during the extended period of offspring development.

• Potential for Distributional Shifts: Viviparous species currently concentrated in cold climates might face pressure to shift their distributions towards cooler areas, such as higher latitudes or elevations, if these remain available and suitable→ shifts might be limited by geographical barriers, competition with existing species, and the physiological tolerances of the viviparous species themselves.

• Evolutionary Responses – Difficulty of Reversal: The sources indicate that while viviparity has evolved multiple times, reversal to oviparity is thought to be exceedingly difficult due to the re-evolution of lost reproductive traits like the egg-shell→ might need to adapt in other ways or face potential declines if they are unable to cope with the altered thermal environment and the persistent costs of viviparity.

• environmental sex determination in crocodiles, lizards and turtles/tortoises
  
  

What evolutionary mechanisms might explain the observed link between viviparity and increased diversification rates in fish?

• Enhanced Colonisation Ability: Viviparous females carry fertilised embryos, allowing a single pregnant female to colonise a new watershed. Unlike oviparous fish, which require at least a pair to establish a population in a new location, a single viviparous female can found a new, geographically isolated population. This increased dispersal capability and establishment success in new geographic regions can lead to geographic isolation, a crucial precursor to speciation. Over time, these isolated populations can diverge genetically and morphologically, eventually leading to the formation of new species.

• Increased Offspring Survival: The young of viviparous species are relatively protected from their environment during development within the mother. This protection can lead to higher survival rates compared to the eggs and larvae of oviparous species, which are exposed to environmental stressors and predation. Higher juvenile survival can facilitate the establishment of new populations in diverse habitats, potentially opening up new ecological niches and driving further diversification.

• The study on squamates highlights that viviparity has evolved multiple times in squamates, suggesting that it is a trait that can arise and potentially influence diversification across different vertebrate lineages. The paper also mentions that viviparous lineages might disperse to and thrive in new environments after the evolution of viviparity, which aligns with the idea of enhanced colonisation as a driver of diversification in fish.

• In contrast to fish, the Helmstetter et al. (2016) paper notes that in reptiles, viviparity has been associated with increased rates of both speciation and extinction, resulting in net diversification rates similar to oviparous groups. This suggests that the relationship between viviparity and diversification can vary across different vertebrate taxa, and the specific mechanisms at play might differ depending on the ecological and evolutionary context.

In summary, in Cyprinodontiformes fish, the increased ability to colonise new areas by single gravid females, higher offspring survival rates due to maternal protection, and the potential for genomic conflicts arising from viviparity are proposed evolutionary mechanisms that could explain the observed link between viviparity and increased diversification rates