Python farming as a flexible and efficient form of agricultural food security.

Diminishing natural resources and increasing climatic volatility are impacting agri-food systems, prompting the need for sustainable and resilient alternatives. Python farming is well established in Asia but has received little attention from mainstream agricultural scientists. We measured growth rates in two species of large pythons (Malayopython reticulatus and Python bivittatus) in farms in Thailand and Vietnam and conducted feeding experiments to examine production efficiencies. Pythons grew rapidly over a 12-month period, and females grew faster than males. Food intake and growth rates early in life were strong predictors of total lifetime growth, with daily mass increments ranging from 0.24 to 19.7 g/day for M. reticulatus and 0.24 to 42.6 g/day for P. bivittatus, depending on food intake. Pythons that fasted for up to 4.2 months lost an average of 0.004% of their body mass per day, and resumed rapid growth as soon as feeding recommenced. Mean food conversion rate for dressed carcasses was 4.1%, with useable products (dressed carcass, skin, fat, gall bladder) comprising 82% of the mass of live animals. In terms of food and protein conversion ratios, pythons outperform all mainstream agricultural species studied to date. The ability of fasting pythons to regulate metabolic processes and maintain body condition enhances food security in volatile environments, suggesting that python farming may offer a flexible and efficient response to global food insecurity.

Sexual dimorphism in aipysurine sea snakes (Elapidae, Hydrophiinae).

The transition from terrestrial to aquatic life by hydrophiine elapid snakes modified targets of natural selection and likely affected sexual selection also. Thus, the shift to marine life also might have affected sexual dimorphism. Our measurements of 419 preserved specimens of six species of aipysurine snakes (genera Emydocephalus and Aipysurus) revealed sexual dimorphism in mean adult snout-vent length (SVL), body width relative to SVL, lengths and widths of heads and tails relative to SVL, and eye diameter relative to head length. Females averaged larger than males in all taxa, and generally were wider-bodied with shorter and wider tails and smaller eyes. For other traits, sexual dimorphism varied among species: for example, relative head length ranged from male-biased to female-biased, and head shape (width relative to length) was highly dimorphic only in A. laevis. The transition to marine life may have eliminated male-male combat (reducing selection for large males) and favoured visual rather than pheromone-based mate-searching (favouring larger eyes in males). Variation in head-size dimorphism may reflect intersexual niche partitioning, with different taxa following different trajectories. Repeated evolutionary transitions from terrestrial to aquatic life in snakes provide a powerful opportunity to explore selective forces on sexually dimorphic traits.

Intraspecific interference retards growth and development of cane toad tadpoles, but those effects disappear by the time of metamorphosis.

Competition among larval anurans can occur via interference as well as via a reduction in per-capita food supply. Previous research on intraspecific interference competition in cane toad (Rhinella marina) tadpoles found conflicting results, with one study detecting strong effects on tadpoles and another detecting no effects on metamorphs. A capacity to recover from competitive suppression by the time of metamorphosis might explain those contrasting impacts. In a laboratory experiment, we found that nine days of exposure to intraspecific interference competition strongly reduced tadpole growth and development, especially when the competing tadpoles were young (early-stage) individuals. Those competitive effects disappeared by the time of metamorphosis, with no significant effect of competition on metamorph body condition, size, larval period or survival. Temporal changes in the impact of competition were not related to tadpole density or to variation in water quality. The ability of larval cane toads to recover from intraspecific interference competition may enhance the invasive success of this species, because size at metamorphosis is a significant predictor of future fitness. Our study also demonstrates a cautionary tale: conclusions about the existence and strength of competitive interactions among anuran larvae may depend on which developmental stages are measured.

Seasonal shifts along the oviparity-viviparity continuum in a cold-climate lizard population.

Squamate embryos require weeks of high temperature to complete development, with the result that cool climatic areas are dominated by viviparous taxa (in which gravid females can sun-bask to keep embryos warm) rather than oviparous taxa (which rely on warm soil to incubate their eggs). How, then, can some oviparous taxa reproduce successfully in cool climates - especially late in summer, when soil temperatures are falling? Near the northern limit of their distribution (in Sweden), sand lizards (Lacerta agilis) shift tactics seasonally, such that the eggs in late clutches complete development more quickly (when incubated at a standard temperature) than do those of early clutches. That acceleration is achieved by a reduction in egg size and by an increase in the duration of uterine retention of eggs (especially, after cool weather). Our results clarify the ability of oviparous reptiles to reproduce successfully in cool climates and suggest a novel advantage to reptilian viviparity in such conditions: by maintaining high body temperatures, viviparous females may escape the need to reduce offspring size in late-season litters.

The things they carried: The pathogenic effects of old and new parasites following the intercontinental invasion of the Australian cane toad (Rhinella marina).

Brought to Australia in 1935 to control agricultural pests (from French Guiana, via Martinique, Barbados, Jamaica, Puerto Rico and Hawai'i), repeated stepwise translocations of small numbers of founders enabled the cane toad (Rhinella marina) to escape many parasites and pathogens from its native range. However, the infective organisms that survived the journey continue to affect the dynamics of the toad in its new environment. In Australia, the native-range lungworm Rhabdias pseudosphaerocephala decreases its host's cardiac capacity, as well as growth and survival, but not rate of dispersal. The lungworm is most prevalent in long-colonised areas within the toads' Australian range, and absent from the invasion front. Several parasites and pathogens of Australian taxa have host-shifted to cane toads in Australia; for example, invasion-front toads are susceptible to spinal arthritis caused by the soil bacterium, Ochrobactrum anthropi. The pentastome Raillietiella frenata has host-shifted to toads and may thereby expand its Australian range due to the continued range expansion of the invasive toads. Spill-over and spill-back of parasites may be detrimental to other host species; however, toads may also reduce parasite loads in native taxa by acting as terminal hosts. We review the impact of the toad's parasites and pathogens on the invasive anuran's biology in Australia, as well as collateral effects of toad-borne parasites and pathogens on other host species in Australia. Both novel and co-evolved pathogens and parasites may have played significant roles in shaping the rapid evolution of immune system responses in cane toads within their invaded range.

Constructing an Invasion Machine: The Rapid Evolution of a Dispersal-Enhancing Phenotype During the Cane Toad Invasion of Australia.

Biological invasions can induce rapid evolutionary change. As cane toads (Rhinella marina) have spread across tropical Australia over an 80-year period, their rate of invasion has increased from around 15 to 60 km per annum. Toads at the invasion front disperse much faster and further than conspecifics from range-core areas, and their offspring inherit that rapid dispersal rate. We investigated morphological changes that have accompanied this dramatic acceleration, by conducting three-dimensional morphometric analyses of toads from both range-core and invasion-front populations. Morphology of heads, limbs, pectoral girdles and pelvic girdles differed significantly between toads from the two areas, ranging from 0.5% to 16.5% difference in mean bone dimensions between populations, with invasion-front toads exhibiting wider forelimbs, narrower hindlimbs and more compact skulls. Those changes plausibly reflect an increased reliance on bounding (multiple short hops in quick succession) rather than separate large leaps. Within an 80-year period, invasive cane toads have converted the basic anuran body plan - which evolved for occasional large leaps to evade predators - into a morphotype better-suited to sustained long-distance travel.

Ecological immunization: in situ training of free-ranging predatory lizards reduces their vulnerability to invasive toxic prey.

In Australia, large native predators are fatally poisoned when they ingest invasive cane toads (Rhinella marina). As a result, the spread of cane toads has caused catastrophic population declines in these predators. Immediately prior to the arrival of toads at a floodplain in the Kimberley region, we induced conditioned taste aversion in free-ranging varanid lizards (Varanus panoptes), by offering them small cane toads. By the end of the 18-month study, only one of 31 untrained lizards had survived longer than 110 days, compared to more than half (nine of 16) of trained lizards; the maximum known survival of a trained lizard in the presence of toads was 482 days. In situ aversion training (releasing small toads in advance of the main invasion front) offers a logistically simple and feasible way to buffer the impact of invasive toads on apex predators.

Differences in developmental strategies between long-settled and invasion-front populations of the cane toad in Australia.

Phenotypic plasticity can enhance a species' ability to persist in a new and stressful environment, so that reaction norms are expected to evolve as organisms encounter novel environments. Biological invasions provide a robust system to investigate such changes. We measured the rates of early growth and development in tadpoles of invasive cane toads (Rhinella marina) in Australia, from a range of locations and at different larval densities. Populations in long-colonized areas have had the opportunity to adapt to local conditions, whereas at the expanding range edge, the invader is likely to encounter challenges that are both novel and unpredictable. We thus expected invasion-vanguard populations to exhibit less phenotypic plasticity than range-core populations. Compared to clutches from long-colonized areas, clutches from the invasion front were indeed less plastic (i.e. rates of larval growth and development were less sensitive to density). In contrast, those rates were highly variable in clutches from the invasion front, even among siblings from the same clutch under standard conditions. Clutches with highly variable rates of growth and development under constant conditions had lower phenotypic plasticity, suggesting a trade-off between these two strategies. Although these results reveal a strong pattern, further investigation is needed to determine whether these different developmental strategies are adaptive (i.e. adaptive phenotypic plasticity vs. bet-hedging) or instead are driven by geographic variation in genetic quality or parental effects.

Delegation to automaticity: the driving force for cognitive evolution?

The ability to delegate control over repetitive tasks from higher to lower neural centers may be a fundamental innovation in human cognition. Plausibly, the massive neurocomputational challenges associated with the mastery of balance during the evolution of bipedality in proto-humans provided a strong selective advantage to individuals with brains capable of efficiently transferring tasks in this way. Thus, the shift from quadrupedal to bipedal locomotion may have driven the rapid evolution of distinctive features of human neuronal functioning. We review recent studies of functional neuroanatomy that bear upon this hypothesis, and identify ways to test our ideas.

Atherosclerosis-susceptible and atherosclerosis-resistant pigeon aortic cells express different genes in vivo.

Spontaneous atherosclerosis in the White Carneau (WC-As) pigeon is inherited as a single gene disorder, and its progression closely mirrors the human disease. Representational difference analysis and microarray were used to identify genes that were differentially expressed between the susceptible WC-As and resistant Show Racer (SR-Ar) aortic tissue. The RNA extracted from 1-d-old squab aortas was used to make cDNA for each experiment. Fifty-six unique genes were found using representational difference analysis, with 25 exclusively expressed in the WC-As, 15 exclusive to the SR-Ar, and 16 nonexclusive genes having copy number variation between breeds. Caveolin and ß-actin were expressed in the WC-As, whereas the proteasome maturation protein and the transcription complex CCR4-NOT were exclusive to the SR-Ar. Microarray analysis revealed 48 genes with differential expression. Vascular endothelial growth factor and p53 binding protein were among the 17 genes upregulated in the WC-As. Thirty-one genes were upregulated in the SR-Ar including the transforming growth factor-ß signaling factor SMAD2 and heat shock protein 90. Genes representing several biochemical pathways were distinctly different between breeds. The most striking divergences were in cytoskeletal remodeling, proteasome activity, cellular respiration, and immune response. Actin cytoskeletal remodeling appears to be one of the first differences between susceptible and resistant breeds, lending support to the smooth muscle cell phenotypic reversion hypothesis of human atherogenesis.

An airborne sex pheromone in snakes.

Most reptile sex pheromones so far described are lipid molecules too large to diffuse through the air; instead, they are detected via direct contact (tongue-flicking) with another animal's body or substrate-deposited trails, using the vomeronasal system. The only non-lipid pheromone reported in snakes involves courtship termination in red-sided gartersnakes (Thamnophis sirtalis parietalis): males that encounter copulatory fluids cease courtship, presumably reflecting the futility of courting an already-mating female. Our field experiments at a communal den in Manitoba show that this pheromone can work via olfaction: courtship is terminated by exposure to airborne scents from mating conspecifics, and does not require direct contact (tongue-flicking). Hence, the sexual behaviour of reptiles can be affected by airborne as well as substrate-bound pheromones.

Are reptile and amphibian species younger in the Northern Hemisphere than in the Southern Hemisphere?

A previous analysis of molecular phylogenies suggested that intraspecific diversification had occurred more recently in temperate-zone Northern Hemisphere reptiles and amphibians than in Southern Hemisphere taxa. Here, we test potential explanations for this pattern. We examined published phylogenetic analyses, derived from genetic sequence data, to generate two estimates of the age of species: (i) the oldest intraspecific diversification event within each taxon and (ii) the inferred timing of the split between two sister species. The timing of splits between species shows the same pattern as splits within species, and thus may be due to climatically driven cladogenic and extinction events or may be an artefact of differing levels of taxonomic knowledge about the fauna. Current rates of species descriptions suggest that many more taxa remain to be described in the Southern Hemisphere than the Northern Hemisphere; for that bias to fully explain our results on species age differences, the proportion of undescribed Southern taxa would need to be ≥ 12% in reptiles and ≥ 51% in anurans. For reptiles, taxonomic ignorance plausibly explains the apparent difference in mean age of species between the Southern and Northern Hemispheres; but this explanation can apply to amphibians only if a vast number of Southern taxa remain to be described.

Fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by female grass snakes, Natrix natrix (Colubridae).

Phenotypic traits of hatchling reptiles are strongly influenced by incubation regimes (e.g. of temperature and moisture), suggesting that maternal choice of suitable nest-sites should be under intense selection. Our laboratory incubation of 209 eggs (17 clutches) from wild-caught Swedish grass snakes (Natrix natrix) showed that scale abnormalities (half-scales on one side of the body, often reflecting lateral asymmetry in the number of ribs) occurred more frequently if eggs were incubated under cooler conditions. Especially at low incubation temperatures, individuals with scale asymmetries took longer to hatch than did symmetric conspecifics, were smaller in body length at hatching and were slower in trials of locomotor speed. Anti-predator tactics also covaried with scale asymmetry. These patterns suggest that individuals with asymmetric scales should have lower fitness and hence should rarely survive to adulthood in the wild. We tested this prediction by examining 201 field-collected snakes from museum collections. As predicted, scale asymmetries were seen primarily in small snakes, and rarely in larger animals. We interpret these data to suggest that scale asymmetries in this species offer an index of developmental instability and that fitness disadvantages to disrupted embryogenesis impose selection against suboptimal nest-site choice by females.

Behavioral responses to immune-system activation in an anuran (the cane toad, Bufo marinus): field and laboratory studies.

The challenges posed by parasites and pathogens evoke behavioral as well as physiological responses. Such behavioral responses are poorly understood for most ectothermic species, including anuran amphibians. We quantified effects of simulated infection (via injection of bacterial lipopolysaccharide [LPS]) on feeding, activity, and thermoregulation of cane toads Bufo marinus within their invasive range in tropical Australia. LPS injection reduced feeding rates in laboratory trials. For toads in outdoor enclosures, LPS injection reduced activity and shifted body temperature profiles. Although previous research has attributed such thermal shifts to behavioral fever (elevated body temperatures may help fight infection), our laboratory studies suggest instead that LPS-injected toads stopped moving. In a thermal gradient, LPS-injected toads thus stayed close to whichever end of the gradient (hot or cold) they were first introduced; the introduction site (rather than behavioral thermoregulation) thus determined body temperature regimes. Shifts in thermal profiles of LPS-injected toads in outdoor enclosures also were a secondary consequence of inactivity. Thus, the primary behavioral effects of an immune response in cane toads are reduced rates of activity and feeding. Thermoregulatory modifications also occur but only as a secondary consequence of inactivity.

Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads.

Human activities are changing habitats and climates and causing species' ranges to shift. Range expansion brings into play a set of powerful evolutionary forces at the expanding range edge that act to increase dispersal rates. One likely consequence of these forces is accelerating rates of range advance because of evolved increases in dispersal on the range edge. In northern Australia, cane toads have increased their rate of spread fivefold in the last 70 years. Our breeding trials with toads from populations spanning the species' invasion history in Australia suggest a genetic basis to dispersal rates and interpopulation genetic variation in such rates. Toads whose parents were from the expanding range front dispersed faster than toads whose parents were from the core of the range. This difference reflects patterns found in their field-collected mothers and fathers and points to heritable variance in the traits that have accelerated the toads' rate of invasion across tropical Australia over recent decades. Taken together with demonstrated spatial assortment by dispersal ability occurring on the expanding front, these results point firmly to ongoing evolution as a driving force in the accelerated expansion of toads across northern Australia.

Insights into the adaptive significance of vertical pupil shape in snakes.

Pupil shape in vertebrates ranges from circular to vertical, with multiple phylogenetic shifts in this trait. Our analyses challenge the widely held view that the vertical pupil evolved as an adaptation to enhance night vision. On functional grounds, a variable-aperture vertical pupil (i) allows a nocturnal species to have a sensitive retina for night vision but avoid dazzle by day by adjusting pupil closure, and (ii) increases visual acuity by day, because a narrow vertical pupil can project a sharper image onto the retina in the horizontal plane. Detection of horizontal movement may be critical for predators that wait in ambush for moving prey, suggesting that foraging mode (ambush predation) as well as polyphasic activity may favour the evolution of vertical pupil shape. Camouflage (disruption of the circular outline of the eye) also may be beneficial for ambush predators. A comparative analysis in snakes reveals significant functional links between pupil shape and foraging mode, as well as between pupil shape and diel timing of activity. Similar associations between ambush predation and vertically slit pupils occur in lizards and mammals also, suggesting that foraging mode has exerted major selective forces on visual systems in vertebrates.

A seasnake's colour affects its susceptibility to algal fouling.

Evolutionary transitions from terrestrial to aquatic life modify selective forces on an animal's coloration. For example, light penetrates differently through water than air, and a new suite of predators and visual backgrounds changes the targets of selection. We suggest that an aquatic animal's coloration may also affect its susceptibility to algal fouling. In a colour-polymorphic field population of seasnakes (Emydocephalus annulatus) in New Caledonia, black individuals supported higher algal cover than did banded conspecifics. In experimental tests, black snake models (plastic tubes) accumulated more algae than did banded models. Algal cover substantially reduced snake activity (in the field) and swimming speeds (in the laboratory). Effects of algal cover on a snake's hydrodynamic efficiency and/or its rate of cutaneous gas exchange thus may impose selection on the colours of aquatic organisms.

Fitness costs may explain the post-colonisation erosion of phenotypic plasticity.

Many organisms can adjust their phenotypes to match local environmental conditions via shifts in developmental trajectories, rather than relying on changes in gene frequencies wrought by natural selection. Adaptive developmental plasticity confers obvious benefits in terms of rapid response and higher mean fitness, so why is it not more common? Plausibly, adaptive plasticity also confers a cost; reshaping the phenotype takes time and energy, so that canalised control of trait values enhances fitness if the optimal phenotype remains the same from one generation to the next. Although this idea is central to interpreting the fitness consequences of adaptive plasticity, empirical data on costs of plasticity are scarce. In Australian tiger snakes, larger relative head size enhances maximal ingestible prey size on islands containing large prey. The trait arises via adaptive plasticity in snake populations on newly colonised islands but becomes genetically canalised on islands where snakes have been present for much longer periods. We experimentally manipulated relative head size in captive neonatal snakes to quantify the costs of adaptive plasticity. Although small-headed snakes were able to increase their head sizes when offered large prey, the delay in doing so, and their inability to consume large prey at the outset, significantly reduced their growth rates relative to conspecifics with larger heads at the beginning of the experiment. This study describes a proximate cause to the post-colonisation erosion of developmental plasticity recorded in tiger snake populations.

Restricted dispersal and genetic diversity in populations of an endangered montane lizard (Eulamprus leuraensis, Scincidae).

Many alpine species are under threat from global climate change, as their geographic ranges become increasingly fragmented and unsuitable. Understanding rates and determinants of gene flow among such fragmented populations, over historical as well as recent timescales, can help to identify populations under threat. It is also important to clarify the degree to which loss of local populations reduces overall genetic diversity within the taxon. The endangered Blue Mountains Water Skink (Eulamprus leuraensis) is restricted to <40 small swamps in montane south-eastern Australia. Our analyses of seven microsatellite loci of 241 animals from 13 populations show strong geographic structure, with major genetic divergence even between populations separated by <0.5 km. Dispersal between populations is scarce, and appears to involve mostly males. Our analyses suggest potential recent bottleneck events in all the identified populations, and lower genetic diversity and population size parameter at lower-elevation sites than at higher-elevation sites. Management of this endangered taxon thus needs to treat most populations separately, because of their genetic distinctiveness and low rates of genetic exchange.

Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards.

The timing of birth is often correlated with offspring fitness in animals, but experimental studies that disentangle direct effects of parturition date and indirect effects mediated via variation in female traits are rare. In viviparous ectotherms, parturition date is largely driven by female thermal conditions, particularly maternal basking strategies. Our field and laboratory studies of a viviparous lizard (Niveoscincus ocellatus) show that earlier-born offspring are more likely to survive through their first winter and are larger following that winter, than are later-born conspecifics. Thus, the association between parturition date and offspring fitness is causal, rather than reflecting an underlying correlation between parturition date and maternal attributes. Survival selection on offspring confers a significant advantage for increased maternal basking in this species, mediated through fitness advantages of earlier parturition. We discuss the roles of environmentally imposed constraints and parent-offspring conflict in the evolution of maternal effects on parturition date.