Predation is a strong selective pressure generating morphological, physiological and behavioural responses in organisms. As predation risk is often higher during juvenile stages, antipredator defences expressed early in life are paramount to survival. Maternal effects are an efficient pathway to produce such defences. We investigated whether maternal exposure to predator cues during gestation affected juvenile morphology, behaviour and dispersal in common lizards (Zootoca vivipara). We exposed 21 gravid females to saurophagous snake cues for one month while 21 females remained unexposed (i.e. control). We measured body size, preferred temperature and activity level for each neonate, and released them into semi-natural enclosures connected to corridors in order to measure dispersal. Offspring from exposed mothers grew longer tails, selected lower temperatures and dispersed thrice more than offspring from unexposed mothers. Because both tail autotomy and altered thermoregulatory behaviour are common antipredator tactics in lizards, these results suggest that mothers adjusted offspring phenotype to risky natal environments (tail length) or increased risk avoidance (dispersal). Although maternal effects can be passive consequences of maternal stress, our results strongly militate for them to be an adaptive antipredator response that may increase offspring survival prospects.
The morphology of organisms is generally well matched to their environment, presumably because expression of their genes is tailored either at the population or the individual level to suit local conditions: for example, snake populations that persistently encounter large prey may accumulate gene mutations that specify a large head size, or head growth may be increased in individual snakes to meet local demands (adaptive developmental plasticity). Here we test the relative contributions of genetics and environment to the jaw sizes of two tiger snake populations: one that consumes small prey on the mainland, and an island population that relies on larger prey and has a larger jaw size. Although the idea of adaptive plasticity in response to environmental pressures is controversial, we find that both factors influence the difference in jaw size between the two populations, and the influence of developmental plasticity is greater in the island population.
In 1942, C.H. Waddington [1] suggested that colonizing populations could initially succeed by flexibly altering their characteristics (phenotypic plasticity; [2-4]) in fitness-inducing traits, but selective forces would rapidly eliminate that plasticity to result in a canalized trait [1, 5, 6]. Waddington termed this process "genetic assimilation"[1, 7]. Despite the potential importance of genetic assimilation to evolutionary changes in founder populations [8-10], empirical evidence on this topic is rare, possibly because it happens on short timescales and is therefore difficult to detect except under unusual circumstances [11, 12]. We exploited a mosaic of snake populations isolated (or introduced) on islands from less than 30 years ago to more than 9000 years ago and exposed to selection for increased head size (i.e., ability to ingest large prey [13-16]). Here we show that a larger head size is achieved by plasticity in "young" populations and by genetic canalization in "older" populations. Island tiger snakes (Notechis scutatus) thus show clear empirical evidence of genetic assimilation, with the elaboration of an adaptive trait shifting from phenotypically plastic expression through to canalization within a few thousand years.
Reproduction is energetically expensive for both sexes, but the magnitude of expenditure and its relationship to reproductive success differ fundamentally between males and females. Males allocate relatively little to gamete production and, thus, can reproduce successfully with only minor energy investment. In contrast, females of many species experience high fecundity-independent costs of reproduction (such as migration to nesting sites), so they need to amass substantial energy reserves before initiating reproductive activity. Thus, we expect that the relationship between energy reserves and the intensity of reproductive behavior involves a threshold effect in females, but a gradual (or no) effect in males. We tested this prediction using captive vipers (Vipera aspis), dividing both males and females into groups of high versus low body condition. Snakes from each group were placed together and observed for reproductive behavior; sex-steroid levels were also measured. As predicted, females in below-average body condition had very low estradiol levels and did not show sexual receptivity, whereas males of all body condition indices had significant testosterone levels and displayed active courtship. Testosterone levels and courtship intensity increased gradually (i.e., no step function) with body condition in males, but high estradiol levels and sexual receptivity were seen only in females with body reserves above a critical threshold. The energetics of reproduction has been a central theme in the ecological study of life history variation (Hirshfield and Tinkle, 1975;Morris, 1987Morris, , 1992Winkler and Wallin, 1987;Stearns, 1992; Monaghan and Nager, 1997), and more recently this topic has become an important focus in behavioral endocrinology (Cherel, Mauget, Lacroix, and Gilles, 1994;Bronson, 1998). It is obvious that organisms cannot reproduce in the total absence of energy reserves (Frish, 1978;Frish and McArthur, 1974), but the relationship between the amount of energy reserves and reproductive output (or effort) is complex and varies among species. In some species there is a linear relationship between energy reserves and reproductive output. In others there appears to be no discernible relationship (e.g., if clutch and offspring sizes are fixed) or a complex nonlinear relationship between the two variables. For example, many organisms are "capital breeders" that rely on previously gathered energy stored in the form of body reserves (i.e., fat bodies, proteins) rather than on current energy intake to fuel the energetically costly process of reproduction (Drent and Daan, 1980;Jö nsson, 1997; Bonnet, Bradshaw, and Shine, 1998). In such species, life history theory predicts that a threshold level of energy reserves is necessary for a reproductive cycle to begin, rather than a linear relationship in which an increment in energy availability adds an increment in reproductive output (Schaffer, 1974;Bull and Shine, 1979;Stearns, 1992). Several empirical studies provide evidence for nonlinear relationships between...
Aim To investigate the influence of tepuian geomorphology on species diversification in the Pantepui biogeographical region based on the phylogenetic relationships and divergence times of tepui‐endemic clades of stefania frogs (Stefania, Hemiphractidae). Location The ‘tepuis’ and uplands/lowlands of the Pantepui biogeographical region of northern South America, one of the least accessible and least studied areas in the world. Methods Two mitochondrial and two nuclear DNA sequences from 60 individuals of Stefania from 24 localities in Pantepui were employed to infer phylogenetic affinities and estimate divergence times within the genus using both concatenation and species tree analyses. Ancestral areas were inferred using multiple models in a common likelihood framework. Results Phylogenetic analyses revealed high diversity in the genus Stefania with 10 candidate species in the Eastern Pantepui District. Four strongly supported clades are recovered in the area, one being exclusively composed of microendemics on isolated tepui summits. Biogeographical analyses suggest episodes of fragmentation of widespread tepuian ancestors from the onset of diversification of the genus, estimated in the Oligocene (c. 26 Ma), therefore suggesting a neglected vicariant model of Pantepui evolution, the Plateau Theory. Main conclusions Although our results suggest that vicariance played an important role in the diversification of Stefania, speciation in Pantepui followed an intricate pattern implying multiple nonexclusive processes. Vicariance and dispersal likely influenced diversification patterns of the Pantepui fauna, possibly according to the following sequence: (1) Cenozoic vicariance; (2) reorganization of species diversity due to periods of climatic instability; (3) recent invasions (Pleistocene) of widespread upland taxa.
In a diverse array of avian and mammalian species, experimental manipulations of clutch size have tested the hypothesis that natural selection should adjust numbers of neonates produced so as to maximize the number of viable offspring at the end of the period of parental care. Reptiles have not been studied in this respect, probably because they rarely display parental care. However, females of all python species brood their eggs until hatching, but they do not care for their neonates. This feature provides a straightforward way to experimentally increase or reduce clutch size to see whether the mean clutch size observed in nature does indeed maximize hatching success and/or optimize offspring phenotypes. Eggs were removed or added to newly laid clutches of Ball Pythons (Python regius) in tropical Africa (nine control clutches, eight with 50% more eggs added, six with 42% of eggs removed). All clutches were brooded by females throughout the 2‐month incubation period. Experimental manipulation of clutch‐size did not significantly affect the phenotypes (morphology, locomotor ability) of hatchlings, but eggs in ‘enlarged’ clutches hatched later, and embryos were more likely to die before hatching. This mortality was due to desiccation of the eggs, with females being unable to cover ‘enlarged’ clutches sufficiently to retard water loss. Our results support the notion of an optimal clutch size, driven by limitations on parental ability to care for the offspring. However, the proximate mechanisms that generate this optimum value differ from those previously described in other kinds of animals. © 2003 The Linnean Society of London. Biological Journal of the Linnean Society 2003, 78, 263–272.
SUMMARYClimate change will result in some areas becoming warmer and others cooler, and will amplify the magnitude of year-to-year thermal variation in many areas. How will such changes affect animals that rely on ambient thermal heterogeneity to behaviourally regulate their body temperatures? To explore this question, we raised 43 captive-born tiger snakes Notechis scutatus in enclosures that provided cold (19-22°C), intermediate (19-26°C) or hot (19-37°C) thermal gradients. The snakes adjusted their diel timing of thermoregulatory behaviour so effectively that when tested 14 months later, body temperatures (mean and maximum), locomotor speeds and anti-predator behaviours did not differ among treatment groups. Thus, the young snakes modified their behaviour to compensate for restricted thermal opportunities. Then, we suddenly shifted ambient conditions to mimic year-to-year variation. In contrast to the earlier plasticity, snakes failed to adjust to this change, e.g. snakes raised at cooler treatments but then shifted to hot conditions showed a higher mean body temperature for at least two months after the onset of the new thermal regime. Hence, thermal conditions experienced early in life influenced subsequent thermoregulatory tactics; the mean selected temperature of a snake depended more upon its prior raising conditions than upon its current thermoregulatory opportunities. Behavioural plasticity thus allows snakes to adjust to suboptimal thermal conditions but this plasticity is limited. The major thermoregulatory challenge from global climate change may not be the shift in mean values (to which our young snakes adjusted) but the increased year-to-year variation (with which our snakes proved less able to deal).
Coping with novel environments may be facilitated by plastic physiological responses that enable survival during environmentally sensitive life stages. We tested the capacity for embryos of the common wall lizard (Podarcis muralis) from low altitude to cope with low-oxygen partial pressure (hypoxia) in an alpine environment. Developing embryos subjected to hypoxic atmospheric conditions (15-16% O sea-level equivalent) at 2,877 m above sea level exhibited responses common to vertebrates acclimatized to or evolutionarily adapted to high altitude: suppressed metabolism, cardiac hypertrophy, and hyperventilation. These responses might have contributed to the unaltered incubation duration and hatching success relative to the ancestral, low-altitude, condition. Even so, hypoxia constrained egg energy utilization such that larger eggs produced hatchlings with relatively low mass. These findings highlight the role of physiological plasticity in maintaining fitness-relevant phenotypes in high-altitude environments, providing impetus to further explore altitudinal limits to ecological diversification in ectothermic vertebrates.
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