In order to maximize fitness, life history traits vary under different environmental pressures31,32. In this study, our results showed that maternal investment strategies differ among altitudes. When the effect of body size is removed, the clutch data across seven B. minshanicus populations indicated that females are more fecund but produce smaller egg sizes at higher altitudes than at lower altitudes. The clutch-by-female size further showed a population-level trade-off between fecundity and egg size.
However, if the outlier population (at 3211 m) was not removed, the clutch data across eight B. minshanicus populations indicated that egg size and clutch volume tend to decrease or increase with increasing altitude (F1, 4.409 = 4.19, P = 0.104) or latitude (F1, 0.926 = 8.47, P = 0.218), while female SVL increased with increasing latitude (F1, 4.784 = 7.84, P = 0.040). Since those results were not consistent among populations in this study, additional research may be needed with more intensive sampling efforts along more geographical gradients.
In this study, female SVL was not significantly positive correlated with latitude or altitude. This result was not consistent with previous evidence considering six populations28. The shorter seasonal period of activity, weaker digestion and lower energy of prey may limit larger body size for appearing at high altitudes or latitudes. Moreover, females living in higher-altitudes must store enough energy during the short activity period in order to survive the harsh and extended winter, which may become more difficult for larger individuals. Therefore, Chen et al. (2013)4 suggested that larger females at high altitudes may be costly.
Life history theory suggests that organisms should allocate the limited energy between growth and development, thus creating a trade-off between growth and development1. The clutch data across seven B. minshanicus populations revealed that clutch attributes (clutch size, egg size, and clutch volume) were positively correlated with female size, revealing that larger females produce more eggs, larger eggs and increase reproductive effort. In fact, most amphibians and reptiles, in general, exhibit this relationship between body size and reproductive output. Thus, it is attributed to positive fecundity selection, where female body size is larger for larger clutches33. Like most ectotherms with indeterminate growth, female B. minshanicus fit the von Bertalanffy’s model28, which describes rapid somatic growth for earlier stages followed by slower growth thereafter. This implies that a larger fraction of energy would be devoted to reproduction as individuals become older34,35, thus resulting in age-specific reproductive output.
In some anurans, larger clutches in high-altitude or latitude populations are due to the larger size of high-altitude or latitude females16,22,36,37. When removing the effect of female body size, females at high altitudes produce relatively fewer clutches, but larger eggs than conspecifics from low altitudes5,16,23,38. However, in this study, after controlling for the effect of female size, higher altitude females had higher fecundity and smaller egg sizes with similar reproductive effort than lower altitudes females, thus the endemic plateau toad has evolved a different breeding strategy. This result was consistent with a previous study39, which showed that the phrynosomatid lizard Phrynosoma cornutum had smaller females at higher latitudes that produced larger clutches but similarly sized eggs when compared to larger females at lower latitudes and removing the effect of female size. It is well known that rainfall can directly affect the abundance of food, and may indirectly affect fecundity by reducing fat stores, which is necessary for development of a holistic egg number40. Females may have more resources for reproduction and clutch production if food availability is higher and physiological stress is lower. Interestingly, in this study, rainfall increases with increasing altitude, indicating higher food availability at higher altitudes. In this case, we speculated that resource may not limit clutch production at higher altitudes. Meanwhile, this species selects rabbit or otter holes as hiding and hibernating sites in the field. In this case, they reduce chances of predation and protect against extreme temperature fluctuations, especially in summer and winter. Additionally, disease and predation tend to decline when increasing altitude41. Thus, we speculate that this species does not allocate as much energy to survive the harsh and extended winter, and suggest females living at high altitudes likely allocate more energy for producing clutches. Similarly, Dobzhansky (1950)42 suggested that r-selection strategies were more likely to appear in changing environments (e.g. temperate and high altitude regions), whereas K-selection more likely to be found in relatively stable situations (e.g. tropics). As a consequence, larger clutch size is regarded as an attribute that populations have evolved through time as an adaptation to their general environment and their ecological niche43,44.
Life-history theory emphasizes that high-altitude females are expected to select for the production larger eggs2,3,4,5,6 because larger eggs or offspring will lead to larger initial sizes, faster growth speeds, higher developmental speeds, or both7,8,9,10,11,12. However, our results showed egg size across seven B. minshanicus populations decreased with increasing altitude, which provide support for the notion that life-history strategies respond to environmental conditions. Similarly, in some instances smaller eggs are better45 or some studies report no significant difference between egg size and altitude46,47. Other studies found that some species with small eggs will increase the number of offspring48, especially in the uncertain larval environment. Additionally, small eggs have a relatively large surface-to-volume ratio and require relatively little oxygen during embryonic development49. In this case, this animal may better be able to adapt to the anoxic environment of the Tibetan Plateau.
Although some studies suggest that trade-offs between clutch size and egg size in amphibians seldom occurs4,50,51,52,53, some previous findings5,9,54,55 support the existence of a trade-off. In this study, although intra-population-level trade-off between fecundity and egg size was uncommon, there was a significant inter-population-level trade-off between fecundity and egg size, suggesting that females producing greater numbers will produce smaller eggs to compensate for the energy put into the greater numbers, which are consistent with the general principle of MacArthur and Wilson’s theory of r-versus K-selection in populations56,57. Moreover, higher altitudes influenced investment in egg size, as suggested by the fact that there were stronger negative effects on egg size than on clutch size and reproductive output. Our data also showed that the strength of the trade-off between clutch size and egg size was not different among altitudes and latitudes. However, theoretical53,58 and empirical9,21,54 studies showed that harsh environments promote larger maternal investment in per-individual offspring to improve survival of individual offspring. For B. minshanicus, at higher altitudes, the advantage associated with producing smaller eggs because of increasing fecundity, which potentially maximizes the number of offspring surviving to reproduction10. Therefore, different environmental pressures will lead to geographical variation in life history traits aimed at maximizing fitness31,32. Bufo minshanicus have evolved a different life history strategy to adapt their environments, which may be inconsistent with our expectations. On the Tibetan Plateau, it appears as though more fecundity and smaller egg size are traits that enhance fitness for this animal.
Source: Ecology - nature.com
