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Egg mass at laying (x‐axis, in grams) relative to offspring mass at hatching (y‐axis, in grams) in squamate species laying variable clutch sizes. Both variables are log10‐transformed. R² = .96
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Viviparity (live‐bearing) has independently evolved from oviparity (egg‐laying) in more than 100 lineages of squamates (lizards and snakes).
We might expect consequent shifts in selective forces to affect per‐brood reproductive investment (RI = total mass of offspring relative to maternal mass) and in the way in which that output is partitioned (nu...
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Squamate reptiles are central for studying phenotypic correlates of evolutionary transitions from oviparity to viviparity because these transitions are numerous, with many of them being recent. Several models of life‐history theory predict that viviparity is associated with increased female size, and thus more female‐biased sexual size dimorphism (...
Citations
... After they laid their eggs, typically within 7 days of capture, the females were re-weighed and then released back at their original capture location. Because we recorded body masses of females at capture and after oviposition we were able to quantify mass loss and hence calculate relative clutch mass (RCM) as mass loss divided by postpartum body mass [29,30]. ...
The physical burden of pregnancy may render females slower and less able to evade predation, favouring a reduction in feeding in order to avoid a reduction in survivorship. Life-history theory predicts that an organism’s optimal level of investment into reproduction depends upon whether or not the associated ‘costs’ (such as a decrease in rate of feeding) increase with higher fecundity. Anorexia during pregnancy is widespread among snakes, but there are few field data on fecundity-dependence of such costs. Over a 23-year period, we recorded reproductive condition and feeding status (based on palpation and production of faeces) for 3778 captures of free-ranging female natricine colubrid snakes (keelbacks, Tropidonophis mairii) in tropical Australia. Pregnancy reduced feeding rates, and that decrease was greatest for females with higher reproductive investment (clutch mass relative to maternal mass). Our long-term data provide the first clear-cut evidence of fecundity-dependent costs of reproduction in free-ranging snakes.
... Determining the costs and adaptive benefits of viviparity is fundamental to understanding why viviparity evolves. Relative to oviparity, viviparity appears to impose more restrictions on female reproductive output and incurs a greater cost per reproductive event (48)(49)(50). Yet viviparity must increase relative fitness in some situations because it has evolved multiple times and persisted over millions of years of evolutionary history (46). ...
Viviparity (live birth) represents a significant evolutionary innovation that has emerged in hundreds of lineages of invertebrate and vertebrate animals. The evolution of this trait from the ancestral state of egg laying has involved complex morphological, behavioral, physiological, and genetic changes, which enable internal development of embryos within the female reproductive tract. Comparable changes have also occurred in oviparous, brooding species that carry developing embryos in locations other than the female reproductive tract. This review explores the taxonomic distribution of vertebrate viviparity and brooding (collectively termed pregnancy), discusses the adaptations associated with internal incubation, and examines hypotheses surrounding the evolution of pregnancy in different lineages. Understanding the mechanisms that have led to the emergence of this trait can illuminate questions about the evolution of reproductive complexity and the processes that led to the emergence of evolutionary innovations that have shaped the remarkable diversity of Earth's fauna.
... These features, along with the absence of a larval stage, make reproductive life histories of oviparous and viviparous squamates effectively comparable. In contrast, life-history comparisons between oviparous and viviparous taxa in fishes or amphibians are often confounded by varying degrees of matrotrophy, superfetation, patterns of larval development, etc. (Bassar et al., 2014;Bisazza, 1993;Blackburn, 2015Blackburn, , 2018Kupfer et al., 2016;Velo-Antón et al., 2015;Wourms & Lombardi, 1992; see also Meiri et al., 2020). Therefore, ecological and phenotypic correlates of viviparity have been predominantly explored in snake and/or lizard models. ...
... The effect of parity mode should therefore be examined jointly with the effects of lineage and climate. While past research on the relationship between life-history traits and parity mode has often accounted for phylogeny, the climatic effects were rarely controlled for quantitatively (but see Horváthová et al., 2013;Meiri et al., 2020;Qualls, 1997;Roitberg et al., 2013Roitberg et al., , 2020. The latter control is important, as climate may strongly affect the SSD variation in squamates both within (Chelini et al., 2021;Roitberg, 2007;Roitberg et al., 2020) and among (Tarr et al., 2019) species. ...
Squamate reptiles are central for studying phenotypic correlates of evolutionary transitions from oviparity to viviparity because these transitions are numerous, with many of them being recent. Several models of life‐history theory predict that viviparity is associated with increased female size, and thus more female‐biased sexual size dimorphism (SSD). Yet, the corresponding empirical evidence is overall weak and inconsistent. The lizard Zootoca vivipara, which occupies a major part of Northern Eurasia and includes four viviparous and two non‐sister oviparous lineages, represents an excellent model for testing these predictions.
We analysed how sex‐specific body size and SSD is associated with parity mode, using body length data for nearly 14,000 adult individuals from 97 geographically distinct populations, which cover almost the entire species' range and represent all six lineages. Our analyses controlled for lineage identity, climatic seasonality (the strongest predictor of geographic body size variation in previous studies of this species) and several aspects of data heterogeneity.
Parity mode, lineage and seasonality are significantly associated with female size and SSD; the first two predictors accounted for 14%–26% of the total variation each, while seasonality explained 5%–7%. Viviparous populations exhibited a larger female size than oviparous populations, with no concomitant differences in male size. The variation of male size was overall low and poorly explained by our predictors.
Albeit fully expected from theory, the strong female bias of the body size differences between oviparous and viviparous populations found in Z. vivipara is not evident from available data on three other lizard systems of closely related lineages differing in parity mode. We confront this pattern with the data on female reproductive traits in the considered systems and the frequencies of evolutionary changes of parity mode in the corresponding lizard families and speculate why the life‐history correlates of live‐bearing in Z. vivipara are distinct.
Comparing conspecific populations, our study provides the most direct evidence for the predicted effect of parity mode on adult body size but also demonstrates that the revealed pattern may not be general. This might explain why across squamates, viviparity is only weakly associated with larger size.
... It has been suggested that these constraints could lead to a reduction in the size or number of offspring in viviparous species compared to their oviparous ancestors (Recknagel and Elmer, 2019). However, a recent study has shown that these traits are not affected by reproductive mode (Meiri et al., 2020). Among the hypotheses put forward to understand this paradox, the importance of the fluids contained in the embryonic membranes is central. ...
... This drastic reduction in the mass of amniotic fluids in viviparous species means that, all else being equal, for a given clutch or litter mass, the number and size of neonates will be greater in viviparous than in oviparous species. Amniotic fluid will be the adaptive variable that allows viviparous species to maintain fecundity and offspring quality, which are determinants of individual fitness (Meiri et al., 2020). ...
... Testing this hypothesis and confronting it with alternative or complementary explanations (Meiri et al., 2020) is particularly difficult due to the lack of data on absolute or relative amniotic fluid volumes. This is particularly true at the time of birth, when the volume of amniotic fluid, which tends to increase during development, reaches its maximum level (Lourdais et al., 2015). ...
The Western Three-toed Skink (Chalcides striatus) is a viviparous species found in arid Mediterranean climates. Using artificial shelters, we captured five pregnant females (snout vent length = 139.2 ± 7.9 mm [SD], 131 to 150 mm; total length = 286.0 ± 9.6 mm, 275 to 292 mm [N = 3, two females with damaged tails]); body mass 15.72 ± 3.89 g, 11.55 to 19.88) and kept them in captivity until parturition. Mean litter size and litter mass were 6.2 ± 1.3 (5 to 8 neonates) and 3.85 ± 0.88 g (2.99 to 5.13 g), respectively. Mean neonatal size and mass were 81.2 ± 4.1 mm (total length = 70 to 90 mm, N = 26) and 0.62 ± 0.07 g (0.49 to 0.82 g, N = 31), respectively. On average, the relative litter mass represented 32 ± 3% (29% to 36%) of the postpartum female body mass. The estimated mass of water lost at birth (total mass loss at parturition minus litter mass) was 0.37 ± 0.39 g (0.00 to 0.98 g), representing 10 ± 8% (0 to 26%) of the individual neonate mass. This low value is in line with that expected for viviparous squamates from arid climates, which is much lower than that observed in oviparous or in viviparous squamates from temperate climates. These results help to fill a gap, as the reproductive output of Chalcides striatus has been poorly documented, but mostly because the importance of extraembryonic water mass has been neglected.
... We retrieved 15 traits of 5836 frog species worldwide from AmphiBIO (V1; Oliveira et al., 2017). We retrieved 17 traits of 7235 lizard species and five traits of 4046 snake species worldwide by harmonising multiple published datasets (Feldman et al., 2015(Feldman et al., , 2016Meiri, 2018;Meiri, Avila, et al., 2020a;Meiri, Feldman, et al., 2020b;Slavenko et al., 2022;Zimin et al., 2022). These traits describe the species' activity time, diet, fecundity, microhabitat preference, mode of reproduction, size and substrate preference (see Tables S2.1-3 in Supporting Information S2). ...
The ever‐increasing and expanding globalisation of trade and transport underpins the escalating global problem of biological invasions. Developing biosecurity infrastructures is crucial to anticipate and prevent the transport and introduction of invasive alien species. Still, robust and defensible forecasts of potential invaders are rare, especially for species without known invasion history. Here, we aim to support decision‐making by developing a quantitative invasion risk assessment tool based on invasion syndromes (i.e., generalising typical attributes of invasive alien species). We implemented a workflow based on ‘Multiple Imputation with Chain Equation’ to estimate invasion syndromes from imputed datasets of species' life‐history and ecological traits and macroecological patterns. Importantly, our models disentangle the factors explaining (i) transport and introduction and (ii) establishment. We showcase our tool by modelling the invasion syndromes of 466 amphibians and reptile species with invasion history. Then, we project these models to amphibians and reptiles worldwide (16,236 species [c.76% global coverage]) to identify species with a risk of being unintentionally transported and introduced, and risk of establishing alien populations. Our invasion syndrome models showed high predictive accuracy with a good balance between specificity and generality. Unintentionally transported and introduced species tend to be common and thrive well in human‐disturbed habitats. In contrast, those with established alien populations tend to be large‐sized, are habitat generalists, thrive well in human‐disturbed habitats, and have large native geographic ranges. We forecast that 160 amphibians and reptiles without known invasion history could be unintentionally transported and introduced in the future. Among them, 57 species have a high risk of establishing alien populations. Our reliable, reproducible, transferable, statistically robust and scientifically defensible quantitative invasion risk assessment tool is a significant new addition to the suite of decision‐support tools needed for developing a future‐proof preventative biosecurity globally.
... 10: 231429 information). Because offspring sizes of oviparous and viviparous squamates are very similar [39], we analysed viviparous and oviparous taxa together. For each species we noted whether it is marine (21 species representing all four marine snake lineages) or not (148 species). ...
Evolutionary shifts from one habitat type to another can clarify selective forces that affect life-history attributes. Four lineages of snakes (acrochordids and three clades within the Elapidae) have invaded marine habitats, and all have larger offspring than do terrestrial snakes. Predation by fishes on small neonates offers a plausible selective mechanism for that shift, because ascending to breathe at the ocean surface exposes a marine snake to midwater predation whereas juvenile snakes in terrestrial habitats can remain hidden. Consistent with this hypothesis, snake-shaped models moving through a coral-reef habitat in New Caledonia attracted high rates of attack by predatory fishes, and small models (the size of neonatal terrestrial snakes) were attacked more frequently than were large models (the size of neonatal sea snakes). Vulnerability to predatory fishes may have imposed strong selection for increased offspring size in marine snakes.
... Likewise, females of most oviparous species of reptiles oviposit when the embryos are relatively small, and most water uptake will occur during incubation; hence the total mass of the embryo is far lower than it will be at hatching (Shine 1983, Shine et al. 2018. We also expect natural selection to optimize the volume and mass of the oviductal package relative to the size of the offspring that it will produce, and the most effective way to do so is to reduce water content (Meiri et al. 2020). Given that constraints of space are likely to be greatest for females that carry their offspring through to full development, we might expect water economy to be most evident in viviparous species. ...
... Given that constraints of space are likely to be greatest for females that carry their offspring through to full development, we might expect water economy to be most evident in viviparous species. Comparative studies show that viviparous squamates allocate less water to the embryo relative to energy content than do oviparous squamates (Bonnet et al. 2017), resulting in a similar total mass per oviductal offspring in species adopting either reproductive mode (Meiri et al. 2020). ...
... Reference (i) Reduction in size of offspring during development in utero relative to size at birth Deposit egg at early embryogenesis, before it swells in size Shine (1983) Reduce water content per offspring in large clutches, and with shift to viviparity Bonnet et al. (2017), Meiri et al. (2020) ...
In many taxa, natural selection favours the ability of a female to accommodate a clutch or litter that is very large relative to her own body, placing a selective premium on traits that increase available abdominal space relative to litter volume. Flexible changes during pregnancy might help to mitigate these constraints. Using ultrasound scanning of captive snakes and snakes captured in the field, we explored such traits in reproducing female vipers (Vipera aspis). First, the anteriormost embryos moved forwards as they swelled during pregnancy, taking up space previously occupied by maternal viscera. Second, the oviductal membrane-bound packages containing embryos changed shape to fit flexibly into thicker vs. thinner parts of the mother’s body. Third, intervertebral spaces increased during pregnancy, allowing the mother’s body to lengthen. Maternal size elongation during pregnancy was reversed shortly after parturition. The decrease in size was closely related to the degree of abdominal displacement and reproductive output and was also evident in field-collected females of three European snakes. In summary, our data suggest that elasticity of the mother’s body and flexibility in packaging of the offspring can mitigate abdominal constraints on maximal litter volume and space competition among siblings.
... In this sense, our models also pointed out that viviparity, rather than oviparity, is related to higher road-kill rates. However, as viviparous and oviparous species (at least among Squamata) do not have significant differences in clutch or offspring sizes (Meiri et al., 2020), relations between these traits do not seem like a feasible hypothesis. This may, however, along with the importance of clutch size in most of our models, indicate the relevance of other reproductive traits for reptile road mortality risks, especially the ones related to reproductive speed (such as maturity age), which have already been related to road-kill risks for other vertebrates (González-Suárez et al., 2018;Grilo et al., 2020Grilo et al., , 2021. ...
Reptiles are an understudied group in road ecology, despite evidence of their high vulnerability to road mortality. Recently, trait-based models have been demonstrated to be valuable tools for explaining and predicting road mortality risks for birds and mammals. The present study aimed to apply such models to reptiles for the first time. We fitted eight random forest regression models, controlling for different survey design variables, to explain 782 empirical road-kill rates for Brazilian reptiles and selected the best-performing model to predict road mortality risks for 572 continental species. The results showed that species that are habitat generalists, omnivorous, viviparous, cathemeral, and have intermediate clutch or litter sizes are at a higher risk of being road-killed. The relationships for other traits included in our models were uncertain, but our findings suggest that population density and species-specific behavioural responses to roads and traffic may play an important role in road mortality risks. Geographical location and survey design variables (especially sampling speed and sampling time) were more important in explaining the variance of the empirical road-kill rates than any of the tested ecological and functional traits. Besides adding evidence of the vulnerability of the Amazon region to vertebrate road-kills, this study highlights some similarities between the relationships identified here and those found for birds and mammals (such as with body mass and habitat breadth). We also corroborate that trait-based models are useful tools to aid in conservation efforts but indicate that they can be biased by the methodologies used to collect empirical data. Future road-kill surveys should therefore use methods specifically designed for reptiles and estimate both observer efficiency and carcass removal rates.
... Effective species recovery strategies (e.g., conservation translocations) often rely upon an understanding of behavior, ecological relationships, and demographics of the focal species (Converse et al., 2013). For example, species reproductive ecology often encompasses traits intertwined with population demographics (Bronikowski & Arnold, 1999;Meiri et al., 2020;Rose, Ersan, et al., 2018). However, much ecological and life history information for T. rufipunctatus is data deficient or limited for this species (USFWS, 2019;Wood et al., 2018), including many aspects of reproductive ecology . ...
... Because litter sizes in 2016 were small (e.g., n ≤ 2), we provide descriptive statistics but omit them from analyses hereafter. Variation in offspring body mass can arise from expiring developmental nutrient transfer (Gregory et al., 1992;Meiri et al., 2020;Stewart, 1992), and omitting measurements within the first few days of life have been useful among congenerics . Therefore, the mean age for offspring body mass measurement across litters was 7.3 days (±1.5). ...
... Empirical parturition and parity data, including intervals and frequencies (i.e., iteroparity), is scant in the T. rufipunctatus literature (Degenhardt et al., 1996;Rossman et al., 1996). We Lillywhite, 2014;Meiri et al., 2020). We also document the first-known entirely ex situ scenarios of birth to maturity to reproduction for T. rufipunctatus-for F1 and F2 generations. ...
Zoo-based (ex situ) conservation breeding programs provide invaluable opportunities to uncover enigmatic behaviors and traits of focal species under managed care, which can support research and conservation management efforts. A suite of factors and a limited range have yielded population declines in the threatened narrow-headed gartersnake (Thamnophis rufipunctatus). Better understanding its cryptic ecology and life history (e.g., reproductive ecology) offers conservation benefits. We analyzed data on courtship behavior, parity and litter size, offspring size, and neonatal growth from an ex situ T. rufipunctatus population at the Phoenix Zoo from 2009 to 2018. Courtship behavior and parturition phenology are likely linked with the North American monsoon season, yet the courtship window may be wider than realized. We document the first instances of interannual iteroparity and multigenerational rearing of successful breeders at the ex situ level. Litter sizes varied but were relative to maternal body mass, suggesting that fecundity may be driven by intrinsic condition (e.g., age and size) of breeding females. Mean offspring body masses were equivalent between sexes, and neonate growth trends were quadratic during their first 9 months. Sexual dimorphism became apparent around 4-5 months age. Much of these data are novel for T. rufipunctatus and provide insight into their reproductive ecology. Phenology of reproductive ecology and body size metrics can guide field surveillance, age estimations, and population ecology monitoring, as well as inform ex situ adaptive management practices. Strategies spanning the ex situ-in situ spectrum are applicable to other imperiled taxa to better inform conservation management decisions.
... the climate per se, but rather the limited duration of the season best fitted for reproduction (Shine, 2014), hence potentially favouring a reproductive strategy that maximizes the number of offspring. However, the present evidence indicates no such trade-off, because oviparous and viviparous species have similar reproductive outputs in seasonal environments (Meiri et al., 2020). Thus, seasonality is not expected to have a relationship with reproductive mode, and we found that it does not have strong or consistent effects. ...
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.
