The Adaptive Signigicance of Reptilian Viviparity in the Tropics: Testing the Maternal Manipulation Hypothesis (original) (raw)
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Reptilian viviparity in cold climates: testing the assumptions of an evolutionary hypothesis
Oecologia, 1983
Viviparity (live-bearing) in reptiles often is interpreted as an adaptation to cold climates. This hypothesis relies on (i) body temperatures of gravid females being higher than soil (nest) temperatures; (ii) embryonic development being accelerated by this temperature difference; and (iii) survivorship of hatchlings being increased if eggs hatch before the advent of cold weather in autumn. I gathered data to test these assumptions, using eight species of scincid lizards in a high-elevation area of southeastern Australia. Due to behavioural thermoregulation, body temperatures of gravid lizards average ca. 7~ higher than soil (nest) temperatures. Oviparous female lizards retain eggs in utero for ca. 50% of development. Laboratory studies show that a temperature increase from 17~ (mean nest temperature) to 24~ (mean lizard temperature) reduces incubation periods of eggs by > 40 days in heliothermic species, and < 20 days in a thigmothermic species. In the field, soil temperatures drop to lethally low levels shortly after the usual time of hatching. Simple calculations show that without the acceleration of development caused by uterine retention, eggs could not hatch prior to the onset of these low temperatures in the field. These results support the major assumptions of the "cold climate hypothesis" for the evolution of reptilian viviparity.
The American Naturalist, 2002
It is notoriously difficult to test hypotheses about the selective forces responsible for major phylogenetic transitions in lifehistory traits, but the evolution of viviparity (live bearing) in reptiles offers an ideal model system. Viviparity has arisen in many oviparous reptile lineages that have invaded colder climates. Thermal advantages (eggs retained within the mother's body will be warmer than those laid in the nest) are almost certainly important, but the actual selective pressures remain controversial. For example, the benefit to retention might involve faster development, protection against freezing, predation, or desiccation, or modification of hatchling phenotypes. I experimentally manipulated incubation regimes of a montane scincid lizard (Bassiana duperreyi, Scincidae) to test these ideas. Eggs maintained in cooler "nests" in the laboratory developed more slowly, were more likely to die before hatching, and produced inferior (small, slow) hatchlings. A 2-wk initial period of higher-temperature incubation (simulating uterine retention, an intermediate step toward viviparity) ameliorated these effects. In the field, I placed eggs in artificial nests at the upper elevational limit of natural nests and also extending a further 100 m higher on the mountain. The results mirrored those in the laboratory: retention at maternal body temperatures accelerated hatching, enhanced hatching success, and increased locomotor speeds of hatchlings. This selective advantage of uterine retention was greater at higher elevations and increased with longer retention. The causal process responsible was prolonged lowtemperature incubation rather than freezing, desiccation, or predation, and both hatching success and hatchling viability were affected. Field experiments that directly recreate selective regimes may thus provide robust tests of adaptationist hypotheses.
Journal of evolutionary biology, 2014
Viviparity, the bearing of live young, has evolved well over 100 times among squamate reptiles. This reproductive strategy is hypothesized to allow maternal control of the foetus' thermal environment and thereby to increase the fitness of the parents and offspring. Two hypotheses have been posited to explain this phenomenon: (i) the cold-climate hypothesis (CCH), which advocates low temperatures as the primary selective force; and (ii) the maternal manipulation hypothesis (MMH), which advocates temperature variability as the primary selective force. Here, we investigate whether climatic and geographic variables associated with the CCH vs. the MMH best explain the current geographical distributions of viviparity in lizards while incorporating recent advances in comparative methods, squamate phylogenetics and geospatial analysis. To do this, we compared nonphylogenetic and phylogenetic models predicting viviparity based on point-of-capture data from 20,994 museum specimens represe...
Females of several lizard species modify their body temperature during pregnancy, probably in connection with the optimisation of hatchling phenotypes. We studied variations in the temperature selected by gravid females compared with those selected by males and non-gravid females in an oviparous population of Zootoca vivipara (Jacquin, 1797) (Squamata: Lacertidae) of Northern Spain and examined the effects of incubation temperature on the phenotypic variation of hatchlings. Cloacal temperatures of gravid females active in the field were lower than those of males and non-gravid females, as well as the temperatures selected in a thermal gradient created in the laboratory (mean 7s.d.: 32.3371.27 1C for gravid females; 34.05 7 1.07 1C for males and non-gravid females). Effects of temperature were assessed by incubating eggs at five constant temperatures (21, 25, 29, 32 and 34 1C). Incubation time decreased as temperature increased, following a negative exponential function. Incubation temperatures also affected the hatchlings' morphology: hatchlings incubated at 34 1C had shorter heads than those from other temperatures. Survival at 34 1C (58%) was significantly lower than at the other temperatures (mean 93%). Pregnant females select lower body temperature, approaching the temperatures that optimise hatchling phenotypes, according to predictions of the maternal manipulation hypothesis on the evolution of viviparity. The shift in preferred temperature by pregnant females would result in only a very short delay, if any, of hatching time and, because the temperature selected by pregnant females is much higher than average temperatures recorded in natural nests of Z. vivipara, egg retention considerably shortens incubation time, according to predictions of the cold-climate hypothesis. Our experimental results indicate that the two main hypotheses on the evolution of viviparity are compatible in our study model.
Life-History Evolution in Reptiles
Annual Review of Ecology, Evolution, and Systematics, 2005
▪ Two consequences of terrestrial ectothermy (low energy needs and behavioral control of body temperatures) have had major consequences for the evolution of reptile life-history traits. For example, reproducing females can manipulate incubation temperatures and thus phenotypic traits of their offspring by retaining developing eggs in utero. This ability has resulted in multiple evolutionary transitions from oviparity to viviparity in cool-climate reptile populations. The spatial and temporal heterogeneity of operative temperatures in terrestrial habitats also has favored careful nest-site selection and a matching of embryonic reaction norms to thermal regimes during incubation (e.g., via temperature-dependent sex determination). Many of the life-history features in which reptiles differ from endothermic vertebrates—such as their small offspring sizes, large litter sizes, and infrequent reproduction—are direct consequences of ectothermy, reflecting freedom from heat-conserving cons...