Determinants of breeding dispersal in the sand lizard, Lacerta agilis, (Reptilia, Squamata)

We studied determinants of breeding dispersal (the distance that an animal shifts its mean home range co-ordinate between reproductive events) in an individually marked population of sand lizards (Lacerta agilis) in south west Sweden during 1987–1991. Female breeding dispersal was not determined by age, size, body condition, or number of partners, and females and males that dispersed further did not experience a higher mortality. However, females with a low reproductive output dispersed further than females that reproduced more successfully, and males that lost in bodily condition dispersed further than males that better maintained body condition. We also looked for relationships between age-differences and band-sharing similarity (DNA fingerprinting = DFP) in three categories of lizards — all females, all males, and males and females — to establish whether males would be likely to mate with close kin. Age-difference was strongly correlated with band-sharing in only one category, males and females. When males were older than females this relationship was not significant. However, when females were older than males, age-difference was strongly correlated with band-sharing. Furthermore, females that were old enough to be the mothers of the courting males shared significantly more bands with these males than did the younger females, including the females of the same age as the males. Although parental-specific DFP bands necessary for establishing paternity among our adult lizards were inaccessible to us, we suggest that our circumstantial evidence strongly suggests that some males mate with their mothers. Males that were more closely related with their neighbours also moved further when we controlled statistically for age and mating success. We suggest that by mating with many partners males not only increase their mating success, but also increase the probability of mating with females with ‘good genes’: mean heterozygosity of parents (as revealed by micro-satellites) were strongly correlated with offspring survival.     

Offspring-driven local dispersal in female sand lizards (Lacerta agilis)

We report on a field study in which determinants of female breeding dispersal (i.e. the shift in the mean home range coordinates between successive breeding events) was investigated. Offspring were released in full sib groups (or half sib ones if there was within-clutch multiple paternity) at a separation distance from the females that varied between 'families'. This allowed for analysis of 'offspring nearness' effects on maternal dispersal. When a female's offspring were released more closely to her, she responded with greater dispersal. Furthermore, when the data set was truncated at 100 m maternal-offspring separation distance at offspring release (because perception at longer distances is likely to be unrealistic), maternal dispersal resulted in greater separation distance between female and offspring in the following year. A corresponding analysis for juveniles revealed no effect of maternal nearness on offspring dispersal but identified a significant effect of clutch size, to our surprise with dispersal declining with increasing clutch size. We discuss this result in a context of the 'public information hypothesis' (reinterpreted for juveniles in a nonsocial foraging species), suggesting that conspecific abundance perhaps acts as an indicator of local habitat quality. Thus, our analysis suggests a microgeographic structuring of the adult female population driven by genetic factors, either through inbreeding avoidance, or from simply avoiding individuals with a similar genotype regardless of their pedigree relatedness, while a nongenetic factor seems more important in their offspring.     

Colonization, genetic diversity, and evolution in the Swedish sand lizard, Lacerta agilis (Reptilia, Squamata)

The Swedish sand lizard ( Lacerta agilis ) is a relict species from the post-glacial warmth period. From the geological history of this region, and more recent data on population fragmentation due to disturbance by man, it can be surmised that the Swedish sand lizards passed through at least one population bottleneck in relatively recent times. We tested this hypothesis by investigating the amount and structuring of genetic variability in six microsatellite loci in ten lizard populations from different parts of Sweden. We contrasted these data against those from a Hungarian population which we have reason to assume strongly resembles the founder population for Swedish sand lizards. The average number of alleles per locus in Sweden was 3.3, and these alleles were common in almost all populations, whereas the average number of alleles in the Hungarian population was 8.0. Likewise, the level of expected heterozygosity was lower in the Swedish populations (0.45) compared to the Hungarian population (0.70). The lower variability in Swedish populations is probably a consequence of a common population bottleneck during the immigration subsequent to the latest glacial period. The remaining variability is strongly subdivided between populations (F_ST=0.30) with the main genetic differences being between rather than within populations. Despite the marked isolation of the populations and the present small population sizes (N= 10–300 adults), the Swedish relict populations show a surprisingly high level of observed heterozygosity, indicating that small population size is probably a recent phenomenon.     

Reptilian myotomal myogenesis-lessons from the sand lizard Lacerta agilis L. (Reptilia, Lacertidae)Update

Reptilian myotomal myogenesis is poorly understood. This paper reports on structural, ultrastructural and immunocytochemical studies of muscle differentiation in sand lizard (Lacerta agilis) embryos. During somitogenesis, the somites are composed of epithelial vesicles with a centrally located somitocoel. At later developmental stages the ventral portion of the somite cortex disaggregates into the sclerotome mesenchyme, while the dorsal wall of the somite differentiates into dermomyotome. At these developmental stages, mononucleated cells of the dermomyotome are Pax3-positive. The dermomyotome layer forms the dorsomedial and ventromedial lips. The myotome is first composed of mono- and then of multinucleated myotubes and small mononucleated cells that occur in the vicinity of the myotubes. These mononucleated cells exhibit low proliferative potential as revealed by the use of PCNA antibody. At subsequent stages of myogenesis the mononucleated cells express Pax7 protein, a marker of satellite cells, and assume ultrastructural features characteristic of satellite cells. Some of the mononucleated cells contribute to muscle growth, being involved in fusion with differentiating muscle fibers. This study revealed similarities of myotomal myogenesis in reptiles to that of other vertebrates.     

Age-dependent inbreeding risk and offspring fitness costs in female black grouse

Dispersal is an important mechanism used to avoid inbreeding. However, dispersal may only be effective for part of an individual's lifespan since, post-dispersal individuals that breed over multiple reproductive events may risk mating with kin of the philopatric sex as they age. We tested this hypothesis in black grouse Tetrao tetrix, and show that yearling females never mated with close relatives whereas older females did. However, matings were not with direct kin suggesting that short-distance dispersal to sites containing kin and subsequent overlap of reproductive lifespans between males and females were causing this pattern. Chick mass was lower when kinship was high, suggesting important fitness costs associated with inbred matings. This study shows that increased inbreeding risk might be a widespread yet rarely considered cost of ageing.     

Ultrastructure of the juxtaglomerular apparatus of the kidney and of the peripolar cells in the sand lizard (Lacerta agilis)

In 9 sand lizards ultrastructure of the juxtaglomerular complex of the kidney has been studied. It is presented as juxtaglomerular cells, situating in the middle tunic of the afferent glomerular arteriole near the vascular pole of the renal corpuscle. Cytoplasm of these cells contains secretory granules at various stages of development: young, maturing and mature, as well as solid corpuscles and myofilaments. In some nephrons primitive forms of the macula densa and the juxtaglomerular island occur. Their presence demonstrates phylogenetically new structural organization of the juxtaglomerular complex in lizards. For the first time in reptilia peripolar cells are found, they are situated on the basal membrane of the external part of the glomerular capsule near the vascular pole of the renal corpuscle. A suggestion is made on their functional interconnection with the juxtaglomerular complex.     

Proximate determinants of telomere length in sand lizards (Lacerta agilis)

Telomeres are repeat sequences of non-coding DNA that cap the ends of chromosomes and contribute to their stability and the genomic integrity of cells. In evolutionary ecology, the main research target regarding these genomic structures has been their role in ageing and as a potential index of age. However, research on humans shows that a number of traits contribute to among-individual differences in telomere length, in particular traits enhancing cell division and genetic erosion, such as levels of free radicals and stress. In lizards, tail loss owing to predation attempts results in a stress-induced shift to a more cryptic lifestyle. In sand lizard (Lacerta agilis) males, telomere length was compromised by tail regrowth in a body size-related manner, so that small males, which already exhibit more cryptic mating tactics, were less affected than larger males. Tail regrowth just fell short of having a significant relationship with telomere length in females, and so did age in males. In females, there was a significant positive relationship between age and telomere length. We conclude that the proximate effect of compromised antipredation and its associated stress seems to have a more pronounced effect in males than in females and that age-associated telomere dynamics differ between the sexes.     

Two forms of AMP deaminase from the lizard (Lacerta agilis) liver

Two molecular forms of AMP deaminase have been revealed by phosphocellulose column chromatography in the liver of uricotelic lizard. The calculated S0.5 value of the purified lizard liver AMP deaminase was 2.5 +/- 0.1 for the form I and 3.6 +/- 0.4 for the form II. Both forms of the enzyme were activated by ATP and ADP but the form II to a much higher extent. GTP activated only the form II and inorganic phosphate inhibited both forms. The occurrence of multiple forms of liver AMP deaminase in uricotelic species, as well as its difference from the mammalian enzyme regulation by GTP is suggested to be connected with the uricotelism in these animals.     

Selection and constraints on offspring size‐number trade‐offs in sand lizards (Lacerta agilis)

The trade‐off between offspring size and number is a central component of life‐history theory, postulating that larger investment into offspring size inevitably decreases offspring number. This trade‐off is generally discussed in terms of genetic, physiological or morphological constraints; however, as among‐individual differences can mask individual trade‐offs, the underlying mechanisms may be difficult to reveal. In this study, we use multivariate analyses to investigate whether there is a trade‐off between offspring size and number in a population of sand lizards by separating among‐ and within‐individual patterns using a 15‐year data set collected in the wild. We also explore the ecological and evolutionary causes and consequences of this trade‐off by investigating how a female's resource (condition)‐ vs. age‐related size (snout‐vent length) influences her investment into offspring size vs. number (OSN), whether these traits are heritable and under selection and whether the OSN trade‐off has a genetic component. We found a negative correlation between offspring size and number within individual females and physical constraints (size of body cavity) appear to limit the number of eggs that a female can produce. This suggests that the OSN trade‐off occurs due to resource constraints as a female continues to grow throughout life and, thus, produces larger clutches. In contrast to the assumptions of classic OSN theory, we did not detect selection on offspring size; however, there was directional selection for larger clutch sizes. The repeatabilities of both offspring size and number were low and we did not detect any additive genetic variance in either trait. This could be due to strong selection (past or current) on these life‐history traits, or to insufficient statistical power to detect significant additive genetic effects. Overall, the findings of this study are an important illustration of how analyses of within‐individual patterns can reveal trade‐offs and their underlying causes, with potential evolutionary and ecological consequences that are otherwise hidden by among‐individual variation.     

Density, social information, and space use in the common lizard (Lacerta vivipara)

Socially acquired information is widespread in the animal kingdom.Many individuals make behavioral decisions based on such socialinformation. In particular, individuals may decide to leaveor select their habitat based on social information. Few studieshave investigated the role of density-related information, apotential social cue about habitat quality in dispersal. Here,we tested for the possibility that the phenotype of intrudercommon lizards (Lacerta vivipara) may inadvertently carry informationabout their natal population density. We found that such informationuse is likely. The behavior of focal lizard was influenced bythe natal population density of the intruder it was interactingwith. This suggests that individuals may use the behavior ofothers to acquire appropriate information about surroundingsand to base spatial decisions on this information. Density-relatedinformation may then affect individual movement decisions andthus metapopulation dynamics.     

Fluctuations in incubation temperature affect incubation duration but not morphology,locomotion and growth of hatchlings in the sand lizard Lacerta agilis (Lacertidae)

Li, H., Zhou, Z.‐S., Ding, G.‐H. and Ji, X. 2011. Fluctuations in incubation temperature affect incubation duration but not morphology, locomotion and growth of hatchlings in the sand lizard Lacerta agilis (Lacertidae). —Acta Zoologica (Stockholm) 00 : 1–8. Studies looking for potential effects of temperature and temperature fluctuations on phenotypic traits of reptile hatchlings have shown species variation, but have not always allowed a distinction between effects of fluctuation per se and temperature extremes themselves. To examine whether incubation temperature fluctuation has a key role in influencing the phenotype of offspring, we incubated eggs of the sand lizard Lacerta agilis at one of the four temperature regimes (27, 27 ± 2, 27 ± 4 and 27 ± 6 °C). We found that: (1) hatchlings incubated under the four temperature regimes did not differ from each other in any of the morphological and physiological traits examined; (2) interactions that included temperature treatment did not affect any trait examined; (3) the mean incubation length was longer in the 27 ± 6 °C treatment than in the other three treatments; and (4) female hatchlings were shorter in head length and width but longer in snout‐vent length as well as abdomen length than males derived from the same‐sized egg. Our data show that both the type and the magnitude of temperature variation can affect incubation length. We found no evidence for phenotypic divergence in responses to temperature fluctuations during incubation and therefore suggest that temperature variation does not affect the phenotype of hatchlings in L. agilis.     

Identification of the linkage group of the Z sex chromosomes of the sand lizard (Lacerta agilis,Lacertidae) and elucidation of karyotype evolution in lacertid lizards

The sand lizard (Lacerta agilis, Lacertidae) has a chromosome number of 2n?=?38, with 17 pairs of acrocentric chromosomes, one pair of microchromosomes, a large acrocentric Z chromosome, and a micro-W chromosome. To investigate the process of karyotype evolution in L. agilis, we performed chromosome banding and fluorescent in situ hybridization for gene mapping and constructed a cytogenetic map with 86 functional genes. Chromosome banding revealed that the Z chromosome is the fifth largest chromosome. The cytogenetic map revealed homology of the L. agilis Z chromosome with chicken chromosomes 6 and 9. Comparison of the L. agilis cytogenetic map with those of four Toxicofera species with many microchromosomes (Elaphe quadrivirgata, Varanus salvator macromaculatus, Leiolepis reevesii rubritaeniata, and Anolis carolinensis) showed highly conserved linkage homology of L. agilis chromosomes (LAG) 1, 2, 3, 4, 5(Z), 7, 8, 9, and 10 with macrochromosomes and/or macrochromosome segments of the four Toxicofera species. Most of the genes located on the microchromosomes of Toxicofera were localized to LAG6, small acrocentric chromosomes (LAG11–18), and a microchromosome (LAG19) in L. agilis. These results suggest that the L. agilis karyotype resulted from frequent fusions of microchromosomes, which occurred in the ancestral karyotype of Toxicofera and led to the disappearance of microchromosomes and the appearance of many small macrochromosomes.     

UV-deprived coloration reduces success in mate acquisition in male sand lizards (Lacerta agilis)

Background

Recent work on animal signals has revealed a wide occurrence of UV signals in tetrapods, in particular birds, but also in lizards (and perhaps other Squamate reptiles). Our previous work on the Swedish sand lizard (Lacerta agilis) has verified, both in correlative selection analyses in the wild and with laboratory and field experiments, the importance of the green ‘badge’ on the body sides of adult males for securing mating opportunities, probably mostly through deterring rival males rather than attracting females. The role of UV in communication has, however, never been examined.

Methodology/Principal Findings

Here we show that when measured immediately after spring skin shedding, there is also signaling in the UV. By UV-depriving the signal (reflectance) with sun block chemicals fixated with permeable, harmless spray dressing, we show that males in the control group (spray dressing only) had significantly higher success in mate acquisition than UV-deprived males.

Conclusions/Significance

These results suggest that at least two colour traits in sand lizards, badge area and UV, contribute to rival deterrence and/or female choice on UV characters, which elevates success in mate acquisition in UV intact male sand lizards.     

Promiscuity in sand lizards (Lacerta agilis) and adder snakes (Vipera berus): causes and consequences

We review postcopulatory phenomena in the Swedish sand lizard (Lacerta agilis) and adder (Vipera berus), and in particular, links between female promiscuity, determinants of paternity, and offspring viability. In both species, females mate multiply and exhibit a positive relationship between the number of partners and offspring viability. We conclude that this relationship is most likely the result of variable genetic compatibility between mates arising from postcopulatory phenomena, predominantly assortative fertilization with respect to parental genotypes. However, males who were more successful at mate acquisition were also more successful in situations of sperm competition, suggesting a possible link between male (diploid and haploid) genetic quality per se and probability of fertilization. Neither the number of partners nor the number of matings influenced the risk of infertility in sand lizards, suggesting that selection for reduced risk of infertility is not a sufficient explanation for maintaining female promiscuity in this population. Finally, we conclude that the relatively low genetic variability exhibited by our study populations may have facilitated detection of genetic benefits compared to more outbred ones. However, recent work derived from outbred populations in other taxa suggest a greater generality of the principles we discuss than previously may have been appreciated.     

Dispersal,kinship and inbreeding in an island population of the Great Tit

We investigated the kinship structure of an island population of the Great Tit (Parus major). Kinship of birds could be inferred by comparing their family trees. Dispersal was also studied to explain the observed pattern of kinship. On the island of Vlieland the tits breed in several wooded areas. Both males and females preferred to breed in their natal area; males did so more strongly than females. Hence gene flow between the areas is restricted. However, within the largest wooded area females showed random dispersal, while males showed a slight tendency to breed near their natal site. The degree of kinship of neighbouring birds is a suitable control group for the relatedness of partners that takes into account the effects of dispersal. In the largest wooded area, birds were on average equally related to their partner and to their neighbours. Moreover, the mean coefficient of kinship between male and female neighbours was equal to the average kinship in this part of the population. We conclude that mating is random with respect to kinship. There is no evidence for avoidance of inbreeding. It is unlikely that kin recognition plays an important role in the process of mate choice in this population of Great Tits. We suggest that ecological factors are the main causes for the observed patterns of dispersal and mating. On the island more female than male immigrants enter the population each year. Incidental data indicate an exchange of birds between the population studied and surrounding populations. Ancestries of immigrants are not known, and indeed a first analysis of all birds, including immigrants, showed that males were more closely related than females. However, differential immigration could not fully explain the observed difference in kinship. The presence of local adaptation in males is suggested as a possible additional cause.     

Phenotype matching and inbreeding avoidance in African elephants

Perhaps the most important 'decision' made by any animal (or plant) is whether to disperse--leave kith and kin, or remain with the familiar and related. The benefits of staying at home are obvious, so dispersal requires an explanation--and the most popular is that dispersal functions to avoid inbreeding depression. Strong support comes from the observation that dispersal is so often sex biased. Simply put, all else being equal members of both sexes should prefer to remain philopatric, but this would lead to inbreeding depression so members of one sex have to disperse. In principle, this link between inbreeding depression and sex-biased dispersal could be broken if individuals recognize close kin and avoid mating with them. Archie et al. (2007) provide one of the most compelling analyses to date of the interaction among inbreeding avoidance, kin recognition and mating strategies in any mammal, clearly showing that elephants recognize even close paternal kin and avoid mating with them. Their important results illuminate the subtleties of elephant inbreeding avoidance as well as illustrate the difficulty of arriving at definitive answers to questions about the evolution of dispersal behaviour.     

Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating

Early field work on naked mole-rats, Heterocephalus glaber, suggestedthat small colonies are rare and that colonies can only formby fissioning of existing colonies. Many researchers expectedthat this would result in extreme inbreeding and high relatednesswithin colonies and would thus explain the evolution of eusocialityin naked mole-rats. Here I report evidence of dispersers andoutbreeding in colonies of wild naked mole-rats that suggeststhat inbreeding is not the system of mating for this speciesand that outbreeding is probably frequent. Wild dispersers havethe same morphology as was reported for dispersers in laboratorycolonies. Low levels of genetic variation in previous moleculargenetic studies of naked mole-rats probably result from theviscous population structure typical of fossorial rodents.     

Geographic variation of life‐history traits in the sand lizard,Lacerta agilis: testing Darwin's fecundity‐advantage hypothesis

The fecundity‐advantage hypothesis (FAH) explains larger female size relative to male size as a correlated response to fecundity selection. We explored FAH by investigating geographic variation in female reproductive output and its relation to sexual size dimorphism (SSD) in Lacerta agilis, an oviparous lizard occupying a major part of temperate Eurasia. We analysed how sex‐specific body size and SSD are associated with two putative indicators of fecundity selection intensity (clutch size and the slope of the clutch size–female size relationship) and with two climatic variables throughout the species range and across two widespread evolutionary lineages. Variation within the lineages provides no support for FAH. In contrast, the divergence between the lineages is in line with FAH: the lineage with consistently female‐biased SSD (L. a. agilis) exhibits higher clutch size and steeper fecundity slope than the lineage with an inconsistent and variable SSD (L. a. exigua). L. a. agilis shows lower offspring size (egg mass, hatchling mass) and higher clutch mass relative to female mass than L. a. exigua, that is both possible ways to enhance offspring number are exerted. As the SSD difference is due to male size (smaller males in L. a. agilis), fecundity selection favouring larger females, together with viability selection for smaller size in both sexes, would explain the female‐biased SSD and reproductive characteristics of L. a. agilis. The pattern of intraspecific life‐history divergence in L. agilis is strikingly similar to that between oviparous and viviparous populations of a related species Zootoca vivipara. Evolutionary implications of this parallelism are discussed.