Length of activity season drives geographic variation in body size of a widely distributed lizard

Understanding the factors that drive geographic variation in life history is an important challenge in evolutionary ecology. Here, we analyze what predicts geographic variation in life‐history traits of the common lizard, Zootoca vivipara, which has the globally largest distribution range of all terrestrial reptile species. Variation in body size was predicted by differences in the length of activity season, while we found no effects of environmental temperature per se. Females experiencing relatively short activity season mature at a larger size and remain larger on average than females in populations with relatively long activity seasons. Interpopulation variation in fecundity was largely explained by mean body size of females and reproductive mode, with viviparous populations having larger clutch size than oviparous populations. Finally, body size‐fecundity relationship differs between viviparous and oviparous populations, with relatively lower reproductive investment for a given body size in oviparous populations. While the phylogenetic signal was weak overall, the patterns of variation showed spatial effects, perhaps reflecting genetic divergence or geographic variation in additional biotic and abiotic factors. Our findings emphasize that time constraints imposed by the environment rather than ambient temperature play a major role in shaping life histories in the common lizard. This might be attributed to the fact that lizards can attain their preferred body temperature via behavioral thermoregulation across different thermal environments. Length of activity season, defining the maximum time available for lizards to maintain optimal performance, is thus the main environmental factor constraining growth rate and annual rates of mortality. Our results suggest that this factor may partly explain variation in the extent to which different taxa follow ecogeographic rules.     

Otolith microstructure reveals consequences for juvenile growth of fractional spawning in an invasive goldfish Carassius auratus (Linnaeus, 1758) population

The consequences of fractional spawning on the early‐life growth rates of invasive goldfish (Carassius auratus) from the Qinghai‐Tibet Plateau were studied using the otolith microstructure of samples collected in June 2011. The effect of the estimated hatching date on the subsequent growth of individual fish was determined by back‐calculating their number of growth days, daily growth rates and the onset of their second growth season. The number of growth days in the first growth season ranged from 93 to 186 days. Following hatching, daily growth rates increased rapidly to a maximum of 0.55 mm days^?1 before declining to 0.09 mm days^?1. The effect of the duration of the first growth season on individuals was significant (P < 0.01), with later spawned fish having faster growth rates. These later spawned fish were, however, still significantly smaller in body length at the end of the first growth season (37 ± 4 mm in late hatched fish vs 55 ± 9 mm in early hatched fish). However, the smaller, later hatched fish started growing earlier in their second growth season than all other fish (P < 0.01) and subsequently achieved larger growth increments (P < 0.01), suggesting that the larger, early‐hatched fish were investing more resources in gonadal growth than somatic growth in their second growth year. Thus, this invasive population revealed considerable plasticity in their early‐life growth rates that were associated with the hatching date, potentially having substantial effects on their development in their second year of life.     

Determinants of Dispersal Distance in Free-Ranging Juvenile Lizards

Dispersal of offspring from their natal site has a critical influence on individual fitness. Although the consequences of dispersal have received much theoretical attention, the determinants of dispersal remain poorly understood for many animals. To address this issue, we marked and released size‐manipulated hatchling lizards (Amphibolurus muricatus; Agamidae) over a 3‐mo period in the field to evaluate the effects of body size and the time of hatching on dispersal distance. Our mark–recapture data indicated that body size and offspring sex had little effect on distances travelled by individuals. However, the timing of hatching had a strong impact; individuals that hatched early in the season dispersed further than did those hatching late. This pattern may allow early‐hatched juveniles to disperse and secure high‐quality habitats before the arrival of later‐hatched conspecific competitors.     

The seasonal timing of oviposition in sand lizards (Lacerta agilis): why early clutches are better

We studied a population of sand lizards (Lacerta agilis) near the northern edge of the species' range in coastal Sweden. We captured, marked, released and recaptured 98 adult female lizards over 5 years. Hatchlings from 146 laboratory-incubated clutches (1279 eggs) from field-caught gravid females were measured, weighed, marked and released at the study site. Female sand lizards usually laid only a single clutch of 4 to 15 eggs each year, but varied considerably in the time of year at which they laid their eggs. Oviposition dates shifted between years depending on weather (basking opportunities), but the relative timing of oviposition was consistent within a given female from year-to-year. The first females to oviposit each year were large animals in good physical condition, that had grown rapidly in previous years. “Early” clutches were larger than “later” clutches, had higher hatching success, and tended to have higher post-hatching survival rates. Offspring from early clutches were larger than “later” hatchlings, and differed in body proportions (probably because seasonal changes in maternal temperatures directly modified offspring phenotypes). Overall, our study documents several strong correlates of the timing of oviposition, and suggests that variation in this trait among females has strong fitness consequences, perhaps related to maternal “quality”. The correlations we observed between oviposition date and other traits that have been invoked as determinants of hatchling survival in reptiles (e.g., hatchling size, body shape, opportunities for multiple mating by the mother) suggest that hypotheses advocating simple causal connections between these traits and hatchling success should be viewed with caution.     

Sibling cannibalism in aphidophagous ladybirds: its impact on sex-dependent development and body weight

Abstract:  The effects of sibling egg cannibalism on sex-dependent development and adult body weight were determined by rearing simultaneously two groups of sibling larvae of ladybirds, viz. Propylea dissecta and Coccinella transversalis individually. The first group included cannibals (i.e. neonates, which took a sibling egg as the first meal and later fed on aphids, Aphis craccivora ) and the other included non-cannibals (reared exclusively on aphids). The cannibal larvae developed faster with heavier adults than non-cannibals. This expedited development and nutritional advantage (increased body weight) was greater in first instars indicating maximum benefit of sibling cannibalism to them. Sibling cannibalism was relatively more advantageous to male than to female ladybirds. Laboratory data predict that the larger size of adults in the field could possibly be the result of sibling egg cannibalism at the neonate level.     

Sex-dependent effects of sibling cannibalism on life history traits of the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae)

To investigate the sex-dependent effects of sibling cannibalism on variations in life history traits, I analysed body size, weight and instar interval in relation to the occurrence of sibling cannibalism in the ladybird beetle Harmonia axyridis. Sibling cannibalism at the time of hatching significantly affected the body size and weight of adults. There was a 2.32% and 1.05% increase in the body size of males and females, respectively, and a 3.55% increase and a 2.30% decrease in their respective body weights. Sibling cannibalism also significantly shortened the total and larval instar intervals, by 4.24% in males and by 1.22% in females, mainly due to shortening of the first instar. These results suggest that the effects of sibling cannibalism on life history traits are sex-differentiated and are greater in males than in females. A simulation of aphid density indicated that shortening the instar interval affected larval survival; the aphid density when the larvae completed development was 39.71% and 10.52% larger for cannibalistic males and females, respectively, than for non-cannibals. These results suggest that sibling cannibalism promotes more rapid development and larger adult size, although the effect was more pronounced in males than in females. Faster development may be adaptive for resource tracking, and the large adult size may increase fecundity in females and mating success in males through female mate choice, both resulting in an increase in the fitness of cannibals.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 349–360.     

Does relaxed predation drive phenotypic divergence among insular populations?

The evolution of striking phenotypes on islands is a well‐known phenomenon, and there has been a long‐standing debate on the patterns of body size evolution on islands. The ecological causes driving divergence in insular populations are, however, poorly understood. Reduced predator fauna is expected to lower escape propensity, increase body size and relax selection for crypsis in small‐bodied, insular prey species. Here, we investigated whether escape behaviour, body size and dorsal coloration have diverged as predicted under predation release in spatially replicated islet and mainland populations of the lizard species Podarcis gaigeae. We show that islet lizards escape approaching observers at shorter distances and are larger than mainland lizards. Additionally, we found evidence for larger between‐population variation in body size among the islet populations than mainland populations. Moreover, islet populations are significantly more divergent in dorsal coloration and match their respective habitats poorer than mainland lizards. These results strongly suggest that predation release on islets has driven population divergence in phenotypic and behavioural traits and that selective release has affected both trait means and variances. Relaxed predation pressure is therefore likely to be one of the major ecological factors driving body size divergence on these islands.     

The interplay between natural and sexual selection in the evolution of sexual size dimorphism in Sceloporus lizards (Squamata: Phrynosomatidae)

Sexual size dimorphism (SSD) evolves because body size is usually related to reproductive success through different pathways in females and males. Female body size is strongly correlated with fecundity, while in males, body size is correlated with mating success. In many lizard species, males are larger than females, whereas in others, females are the larger sex, suggesting that selection on fecundity has been stronger than sexual selection on males. As placental development or egg retention requires more space within the abdominal cavity, it has been suggested that females of viviparous lizards have larger abdomens or body size than their oviparous relatives. Thus, it would be expected that females of viviparous species attain larger sizes than their oviparous relatives, generating more biased patterns of SSD. We test these predictions using lizards of the genus Sceloporus. After controlling for phylogenetic effects, our results confirm a strong relationship between female body size and fecundity, suggesting that selection for higher fecundity has had a main role in the evolution of female body size. However, oviparous and viviparous females exhibit similar sizes and allometric relationships. Even though there is a strong effect of body size on female fecundity, once phylogenetic effects are considered, we find that the slope of male on female body size is significantly larger than one, providing evidence of greater evolutionary divergence of male body size. These results suggest that the relative impact of sexual selection acting on males has been stronger than fecundity selection acting on females within Sceloporus lizards.     

Sex-specific niche partitioning and sexual size dimorphism in Australian pythons (Morelia spilota imbricata)

Sexual dimorphism is usually interpreted in terms of reproductive adaptations, but the degree of sex divergence also may be affected by sex-based niche partitioning. In gape-limited animals like snakes, the degree of sexual dimorphism in body size (SSD) or relative head size can determine the size spectrum of ingestible prey for each sex. Our studies of one mainland and four insular Western Australian populations of carpet pythons ( Morelia spilota ) reveal remarkable geographical variation in SSD, associated with differences in prey resources available to the snakes. In all five populations, females grew larger than males and had larger heads relative to body length. However, the populations differed in mean body sizes and relative head sizes, as well as in the degree of sexual dimorphism in these traits. Adult males and females also diverged strongly in dietary composition: males consumed small prey (lizards, mice and small birds), while females took larger mammals such as possums and wallabies. Geographic differences in the availability of large mammalian prey were linked to differences in mean adult body sizes of females (the larger sex) and thus contributed to sex-based resource partitioning. For example, in one population adult male snakes ate mice and adult females ate wallabies; in another, birds and lizards were important prey types for both sexes. Thus, the high degree of geographical variation among python populations in sexually dimorphic aspects of body size and shape plausibly results from geographical variation in prey availability.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 113–125.     

Body-size effect on egg size in eublepharid geckos (Squamata: Eublepharidae), lizards with invariant clutch size: negative allometry for egg size in ectotherms is not universal

Within a single clutch, smaller species of ectotherms generally lay a smaller number of relatively larger eggs than do larger species. Many hypotheses explaining both the interspecific negative allometry in egg size and egg size–number trade-off postulate the existence of an upper limit to the egg size of larger species. Specifically, in lizards, large eggs of large species could have too long a duration of incubation, or they could be too large to pass through the pelvic opening, which is presumably constrained mechanically in larger species. Alternatively, negative allometry could be a result of limits affecting eggs of smaller species. Under the latter concept, hatchling size in smaller species may be close to the lower limit imposed by ecological interactions or physiological processes, and therefore smaller species have to invest in relatively larger offspring. Contrary to these lower limit hypotheses, explanations based on the existence of an upper limit always predict negative egg-size allometry even in animals with invariant clutch size, in which naturally there is no egg size–number trade-off. We studied egg-size allometry in lizards of the family Eublepharidae, a monophyletic group of primitive geckos with large variance in body size and an invariant number of two eggs per clutch. We found an isometric relationship between egg and female size that does not support the upper limit hypotheses.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 527–532.     

Does ‘gliding while gravid’ explain Rensch's rule in flying lizards?

Among species with sexual size dimorphism (SSD), taxa in which males are the larger sex have increasing SSD with increasing body size, whereas in taxa in which females are the larger sex, SSD decreases with body size: Rensch's rule. We show in flying lizards, a clade of mostly female‐larger species, that SSD increases with body size, a pattern similar to that in clades with male‐biased SSD or more evenly mixed SSD. The observed pattern in Draco appears due to SSD increasing with evolutionary changes in male body size; specifically divergence in body size among species that are in sympatric congeneric assemblages. We suggest that increasing body size, resulting in decreased gliding performance, reduces the relative gliding cost of gravidity in females, and switches sexual selection in males away from a small‐male, gliding advantage and toward selection on large size and fighting ability as seen in many other lizards. Thus, selection for large females is likely greater than selection for large males at the smaller end of the body size continuum, whereas this relationship reverses for species at the larger end of the continuum. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 270–282.     

Environmentally cued hatching in reptiles

Evidence is accumulating for the widespread occurrence of environmentally cued hatching (ECH) in animals, but its diversity and distribution across taxa are unknown. Herein I review three types of ECH in reptiles: early hatching, delayed hatching, and synchronous hatching. ECH is currently known from 43 species, including turtles, crocodilians, lizards, snakes, tuatara, and possibly worm lizards. Early hatching caused by physical disturbance (e.g., vibrations) is the most commonly reported ECH across all groups; although it apparently serves an antipredator function in some species, its adaptive value is unknown in most. Delayed hatching, characterized by metabolic depression or embryonic aestivation, and sometimes followed by a hypoxic cue (flooding), occurs in some turtles and possibly in monitor lizards and crocodilians; in some of these species delayed hatching serves to defer hatching from the dry season until the more favorable conditions of the wet season. Synchronous hatching, whereby sibling eggs hatch synchronously despite vertical thermal gradients in the nest, occurs in some turtles and crocodilians. Although vibrations and vocalizations in hatching-competent embryos can stimulate synchronous hatching, cues promoting developmentally less advanced embryos to catch up with more advanced embryos have not been confirmed. Synchronous hatching may serve to dilute predation risk by promoting synchronous emergence or reduce the period in which smells associated with hatching can attract predators to unhatched eggs. Within species, advancing our understanding of ECH requires three types of studies: (1) experiments identifying hatching cues and the plastic hatching period, (2) experiments disentangling hypotheses about multiple hatching cues, and (3) investigations into the environmental context in which ECH might evolve in different species (major predators or abiotic influences on the egg, embryo, and hatchling). Among species and groups, surveys for ECH are required to understand its evolutionary history in reptiles. The probability of ECH occurring is likely influenced by a species's life history, ecology, behavior, and interrelationships with other species (e.g., sizes of predator and prey). More broadly, the discovery of embryo-embryo communication as a mechanism for synchronous hatching in crocodilians and turtles indicates that the social behavior of (nonavian) reptiles has been underestimated.     

Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature‐dependent sex determination

Abstract The jacky dragon, Amphibolurus muricatus (White, ex Shaw 1790) is a medium sized agamid lizard from the southeast of Australia. Laboratory incubation trials show that this species possesses temperature‐dependent sex determination. Both high and low incubation temperatures produced all female offspring, while varying proportions of males hatched at intermediate temperatures. Females may lay several clutches containing from three to nine eggs during the spring and summer. We report the first field nest temperature recordings for a squamate reptile with temperature‐dependent sex determination. Hatchling sex is determined by nest temperatures that are due to the combination of daily and seasonal weather conditions, together with maternal nest site selection. Over the prolonged egg‐laying season, mean nest temperatures steadily increase. This suggests that hatchling sex is best predicted by the date of egg laying, and that sex ratios from field nests will vary over the course of the breeding season. Lizards hatching from eggs laid in the spring (October) experience a longer growing season and should reach a larger body size by the beginning of their first reproductive season, compared to lizards from eggs laid in late summer (February). Adult male A. muricatus attain a greater maximum body size and have relatively larger heads than females, possibly as a consequence of sexual selection due to male‐male competition for territories and mates. If reproductive success in males increases with larger body size, then early hatching males may obtain a greater fitness benefit as adults, compared to males that hatch in late summer. We hypothesize that early season nests should produce male‐biased sex ratios, and that this provides an adaptive explanation for temperature‐dependent sex determination in A. muricatus.     

Bergmann's Rule rules body size in an ectotherm: heat conservation in a lizard along a 2200‐metre elevational gradient

Bergmann's Rule predicts larger body sizes in colder habitats, increasing organisms' ability to conserve heat. Originally formulated for endotherms, it is controversial whether Bergmann's Rule may be applicable to ectotherms, given that larger ectotherms show diminished capacity for heating up. We predict that Bergmann's Rule will be applicable to ectotherms when the benefits of a higher conservation of heat due to a larger body size overcompensate for decreased capacity to heating up. We test this hypothesis in the lizard Psammodromus algirus, which shows increased body size with elevation in Sierra Nevada (SE Spain). We measured heating and cooling rates of lizards from different elevations (from 300 to 2500 m above sea level) under controlled conditions. We found no significant differences in the heating rate along an elevational gradient. However, the cooling rate diminished with elevation and body size: highland lizards, with larger masses, have a higher thermal inertia for cooling, which allows them to maintain heat for more time and keep a high body temperature despite the lower thermal availability. Consequently, the net gaining of heat increased with elevation and body size. This study highlights that the heat conservation mechanism for explaining Bergmann's Rule works and is applicable to ectotherms, depending on the thermal benefits and costs associated with larger body sizes.     

Functional basis for sexual differences in bite force in the lizard Anolis carolinensis

In many species of lizards, males attain greater body size and have larger heads than female lizards of the same size. Often, the dimorphism in head size is paralleled by a dimorphism in bite force. However, the underlying functional morphological basis for the dimorphism in bite force remains unclear. Here, we test whether males are larger, and have larger heads and bite forces than females for a given body size in a large sample of Anolis carolinensis . Next, we test if overall head shape differs between the sexes, or if instead specific aspects of skull shape can explain differences in bite force. Our results show that A. carolinensis is indeed dimorphic in body and head size and that males bite harder than females. Geometric morphometric analyses show distinct differences in skull shape between males and females, principally reflecting an enlargement of the jaw adductor muscle chamber. Jaw adductor muscle mass data confirm this result and show that males have larger jaw adductors (but not jaw openers) for a given body and head size. Thus, the observed dimorphism in bite force in A. carolinensis is not merely the result of an increase in head size, but involves distinct morphological changes in skull structure and the associated jaw adductor musculature.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 111–119.     

Ontogenetic divergence of growth among rainbow smelt morphotypes

Multiple, sympatric morphotypes of rainbow smelt (Osmerus mordax) are known in Lake Utopia, New Brunswick. The largest, ‘giant’ form is predominantly a piscivore, the smaller, ‘dwarf’ form are predominantly planktivores, and there is an intermediate body-sized form. The forms exhibit some genetic variability, but it is body size that best defines morphotypes, trophic status, and spawning behaviour. We compared egg size, spawning date, incubation time, size at hatching, and daily and annual growth to determine when divergence in body size occurs among morphotypes. Giant form larvae hatched earlier and grew faster during their first year. Dwarf and intermediate form larvae displayed inter-annual variability in degree of overlap and divergence in growth which occurred in their first growing season or at age 1+ or 2+. We conclude that earlier hatching, early growth trajectories, and later niche shifting are linked to the persistence of morphotypes, i.e., the process is controlled by the environment and sustained to some degree by spawning segregation.     

Determinants of survival in juvenile Psammodromus algirus lizards

Theories posit that the relative mortality rate of adults and juveniles is a major determinant of population dynamics and life history evolution. Moreover, differential survival of pre-reproductive individuals may be an important source of variation in lifetime reproductive success, and characters that influence survival of juveniles are likely to be under strong selection. We examined survival from hatching to maturity in a natural population of Psammodromus algirus lizards using data from a capture-mark-recapture study. We found that mortality from hatching to maturity was high: only 8% of males and 14% of females that hatched in 1996 survived the entire study period until maturity in spring 1998. The probability of survival was 75% during both the first and second overwinter periods when lizards were inactive most of the time, and about 25% during their first spring to autumn activity season. Our analyses further revealed significant associations between survival and snout-vent length, body condition, sex and microhabitat use. However, the relationship between survival and morphological characters varied among time periods, presumably because the sources of mortality during the activity season were different from those during hibernation. The association between survival and body condition also varied within time periods, both between large and small individuals and between the two sexes. This suggests that the relative importance of different selective agents may change during the life of individuals and vary between males and females due to differences in body size and behaviour. Received: 24 March 1999 / Accepted: 14 February 2000     

Broad-scale patterns of body size in squamate reptiles of Europe and North America

Aim  To document geographical interspecific patterns of body size of European and North American squamate reptile assemblages and explore the relationship between body size patterns and environmental gradients.
Location  North America and western Europe.
Methods  We processed distribution maps for native species of squamate reptiles to document interspecific spatial variation of body size at a grain size of 110 × 110 km. We also examined seven environmental variables linked to four hypotheses possibly influencing body size gradients. We used simple and multiple regression, evaluated using information theory, to identify the set of models best supported by the data.
Results  Europe is characterized by clear latitudinal trends in body size, whereas geographical variation in body size in North America is complex. There is a consistent association of mean body size with measures of ambient energy in both regions, although lizards increase in size northwards whereas snakes show the opposite pattern. Our best models accounted for almost 60% of the variation in body size of lizards and snakes within Europe, but the proportions of variance explained in North America were less than 20%.
Main conclusions  Although body size influences the energy balance of thermoregulating ectotherms, inconsistent biogeographical patterns and contrasting associations with energy in lizards and snakes suggest that no single mechanism can explain variation of reptile body size in the northern temperate zone.     

Sex and environmental sensitivity in blue tit nestlings

In birds and mammals with sexual size dimorphism (SSD), the larger sex is typically more sensitive to adverse environmental conditions, such as food shortage, during ontogeny. However, some recent studies of altricial birds have found that the larger sex is less sensitive, apparently because large size renders an advantage in sibling competition. Still, this effect is not an inevitable outcome of sibling competition, because several studies of other species of altricial birds have found the traditional pattern. We investigated if the sexes differ in environmental sensitivity during ontogeny in the blue tit, a small altricial bird with c. 6% SSD in body mass (males larger than females). We performed a cross-fostering and brood size manipulation experiment during 2 years to investigate if the sexes were differently affected as regards body size (body mass, tarsus and wing length on day 14 after hatching) and pre-fledging survival. We also investigated if the relationship between body size and post-fledging survival differed between the sexes. Pre-fledging mortality was higher in enlarged than in reduced broods, representing poor and good environments, respectively, but the brood size manipulation did not affect the mortality rate of males and females differently. In both years, both males and females were smaller on day 14 after hatching in enlarged as compared to reduced broods. In one of the years, we also found significant Sex × Experiment interactions for body size, such that females were more affected by poor environmental conditions than that of males. Body size was positively correlated with post-fledging survival, but we found no interactive effects of sex and morphological traits on survival. We conclude that in the blue tit, females (the smaller sex) are more sensitive to adverse environmental conditions which, in our study, was manifest in terms of fledgling size. A review of published studies of sex differences in environmental sensitivity in sexually size-dimorphic altricial birds suggests that the smaller sex is more sensitive than the larger sex in species with large brood size and vice versa.     

Anthropogenically modified habitats favor bigger and bolder lizards

Anthropogenic activities often create distinctive but discontinuously distributed habitat patches with abundant food but high risk of predation. Such sites can be most effectively utilized by individuals with specific behaviors and morphologies. Thus, a widespread species that contains a diversity of sizes and behavioral types may be pre‐adapted to exploiting such hotspots. In eastern Australia, the giant (to >2 m) lizard Varanus varius (lace monitor) utilizes both disturbed (campground) and undisturbed (bushland) habitats. Our surveys of 27 sites show that lizards found in campgrounds tended to be larger and bolder than those in adjacent bushland. This divergence became even more marked after the arrival of a toxic invasive species (the cane toad, Rhinella marina) caused high mortality in larger and bolder lizards. Some of the behavioral divergences between campground and bushland lizards may be secondary consequences of differences in body size, but other habitat‐associated divergences in behavior are due to habituation and/or nonrandom mortality.