Natural parasites in conjunction with behavioral and color traits explain male agonistic behaviors in a lizard.

Male competition conforms to a cost-benefit model, because while aggression may increase reproductive prospects, it can also increase the risk of injury. We hypothesize that an additional cost in aggressive males would be an increase in parasite load associated with a high energy investment into sexual competition. Some of these infections, in turn, may downmodulate the level of host aggression via energetic trade-offs. We staged dyadic male contests in the lab to investigate the relationships of multiple parasites with the agonistic behavior of lizard hosts, Sceloporus occidentalis. We also included both color and behavioral traits from opponents in the analyses because (1) color patches of lizards may serve as intraspecific signals used by conspecifics to assess the quality of opponents, and (2) contests between male lizards fit classical models of escalated aggression, where lizards increase aggression displays in response to an opponent's behavior. The results conform to our hypothesis because male lizards displayed more pushups when they had more ticks. Moreover, some parasites may modulate the levels of aggression because lizards infected by hematic coccidians performed fewer pushups. Interestingly, lizards also displayed fewer pushups when both the chroma and size of the opponent's blue patch were greater. The results thus also supported the role of the blue patch of S. occidentalis as a sexual armament, because it contributed to the deterrence of aggression from opponent lizards. We revealed that natural parasitic infections in lizard hosts can contribute to their agonistic behavior. We encourage future studies to account for parasites in behavioral tests with lizards.

Multiple color patches and parasites in Sceloporus occidentalis: differential relationships by sex and infection.

Parasites generally have a negative influence on the color expression of their hosts. Sexual selection theory predicts resistant high-quality individuals should show intense coloration, whereas susceptible low-quality individuals would show poor coloration. However, intensely colored males of different species of Old and New World lizards were more often infected by hemoparasites. These results suggest that high-quality males, with intense coloration, would suffer higher susceptibility to hemoparasites. This hypothesis remains poorly understood and contradicts general theories on sexual selection. We surveyed a population of Sceloporus occidentalis for parasites and found infections by the parasite genera Lankesterella and Acroeimeria. In this population, both males and females express ventral blue and yellow color patches. Lankesterella was almost exclusively infecting males. The body size of the males significantly predicted the coloration of both blue and yellow patches. Larger males showed darker (lower lightness) blue ventral patches and more saturated yellow patches that were also orange-skewed. Moreover, these males were more often infected by Lankesterella than smaller males. The intestinal parasite Acroeimeria infected both males and females. The infection by intestinal parasites of the genus Acroeimeria was the best predictor for the chroma in the blue patch of the males and for hue in the yellow patch of the females. Those males infected by Acroeimeria expressed blue patches with significantly lower chroma than the uninfected males. However, the hue of the yellow patch was not significantly different between infected and uninfected females. These results suggest a different effect of Lankesterella and Acroeimeria on the lizards. On the one hand, the intense coloration of male lizards infected by Lankesterella suggested high-quality male lizards may tolerate it. On the other hand, the low chroma of the blue coloration of the infected males suggested that this coloration could honestly express the infection by Acroeimeria.

Phylogenetic analyses reveal that Schellackia parasites (Apicomplexa) detected in American lizards are closely related to the genus Lankesterella: is the range of Schellackia restricted to the Old World?

BACKGROUND: Species of Schellackia Reichenow, 1919 have been described from the blood of reptiles distributed worldwide. Recently, Schellackia spp. detected in European and Asian lizards have been molecularly characterised. However, parasites detected in American lizard hosts remain uncharacterised. Thus, phylogenetic affinities between the Old and New World parasite species are unknown. METHODS: In the present study, we characterised morphologically and molecularly the hemococcidian parasites (sporozoites) that infect three lizard hosts from North America and two from South America. RESULTS: In total, we generated 12 new 18S rRNA gene sequences of hemococcidian parasites infecting New World lizard hosts. By the microscopic examination of the smears we identified Schellackia golvani Rogier & Landau, 1975 (ex Anolis carolinensis Voigt) and Schellackia occidentalis Bonorris & Ball, 1955 (ex Uta stansburiana Baird & Girard and Sceloporus occidentalis Baird & Girard) in some samples, but the phylogenetic analysis indicated that all 18S rDNA sequences are distant from Schellackia species found in Old World lizards. In fact, the hemococcidian parasites detected in the New World lizards (including S. occidentalis and S. golvani) were closely related to the genus Lankesterella Labbé, 1899. Consequently, we suggest these two species to be included within the genus Lankesterella. CONCLUSIONS: Life history traits of hemococcidian parasites such as the type of host blood cells infected, host species or number of refractile bodies are not valid diagnostic characteristics to differentiate the parasites between the genera Schellackia and Lankesterella. Indeed, lankesterellid parasites with a different number of refractile bodies had a close phylogenetic origin. Based on the phylogenetic results we provide a systematic revision of the North American hemococcidians. Our recommendation is to include the species formerly described in the genus Schellackia that infect American lizards into Lankesterella (Lankesterellidae) as Lankesterella golvani (Rogier & Landau, 1975) n. comb and L. occidentalis (Bonorris & Ball, 1955) n. comb.

Evolutionary games, climate and the generation of diversity.

Environmental stochasticity and climate affect outcomes in evolutionary games, which can thereby affect biological diversity. Our maximum likelihood (ML) estimates of replicator dynamics for morph frequency data from control (25 years) and three experimentally perturbed populations (14 years) of side-blotched lizards yield a 3 × 3 payoff matrix in the generalized Rock-Paper-Scissors family; it has intransitive best replies, and each strategy is its own worst reply. ML estimates indicate significant interactive effects of density and temperature on morph frequency. Implied dynamics feature a powerful interior attractor and recover (for the first time) observed 4-5 year oscillations. Our evolutionary experiment on morph frequency confirms that oscillations are driven by frequency dependent selection, but climate entrains the cycles across the perturbed and control populations within 10 generations. Applying the model across the species range, we find that climate also accounts for morph fixation and mating system diversity, suggesting climate may similarly impact ecosystem diversity.

Does thermal ecology influence dynamics of side-blotched lizards and their micro-parasites?

Hosts and parasites form interacting populations that influence each other in multiple ways. Their dynamics can also be influenced by environmental and ecological factors. We studied host-parasite dynamics in a previously unexplored study system: side-blotched lizards and their micro-parasites. Compared with uninfected lizards, the infected lizards elected to bask at lower temperatures that were outside their range of preferred temperatures. Infected lizards also were not as precise as uninfected lizards in maintaining their body temperatures within a narrow range. At the ecological scale, areas with higher infection rates coincided with more thermally heterogeneous microhabitats as well as with the areas where lizards tended to live longer. Thermal heterogeneity of lizards' microhabitats may provide important clues to the spatial and temporal distribution of infections.

Evidence of maternal effects on temperature preference in side-blotched lizards: implications for evolutionary response to climate change.

Natural populations respond to selection pressures like increasing local temperatures in many ways, including plasticity and adaptation. To predict the response of ectotherms like lizards to local temperature increase, it is essential to estimate phenotypic variation in and determine the heritability of temperature-related traits like average field body temperature (T b) and preferred temperature (T p). We measured T p of Uta stansburiana in a laboratory thermal gradient and assessed the contribution of sex, reproductive status and throat color genotype to phenotypic variation in T b of adult lizards. Females had higher T p than males. However, they temporarily preferred lower temperature when gravid than when nongravid. Using a nested half-sib design for genetic crosses in the laboratory, we estimated relative contributions of additive genetic variation and maternal effects to T p of hatchlings. Our results show that maternal effects, but not additive genetic variation, influence T p of hatchlings in U. stansburiana. Maternal T p and the presence or absence of blue throat color alleles significantly influenced T p of hatchlings. We discuss ecological and evolutionary consequences of these maternal effects in the context of rapid climate change and natural selection that we measure on progeny survival to maturity as a function of maternal T p.

Selection on the timing of adult emergence results in altered circadian clocks in fruit flies Drosophila melanogaster.

To investigate whether circadian clocks in fruit flies Drosophila melanogaster evolve as a consequence of selection on the timing of adult emergence, we raised four replicate populations each of early (early(1..4)) and late (late(1..4)) emerging flies by selecting for adults that emerged during the morning and the evening hours. We estimated the percentage of flies that emerged during the two selection windows to evaluate the direct response to selection, and the circadian phenotypes of adult emergence and locomotor activity rhythms under light/dark (LD) and constant darkness (DD) to assess the correlated response to selection. After 55 generations, the percentage of flies emerging during the morning window increased in the early populations, but decreased in the late populations. The percentage of flies emerging during the evening window increased in the late populations, but decreased in the early populations. The time course and waveform of emergence and locomotor activity rhythms of the selected populations diverged from each other as well as from the controls. Further, the circadian periodicity of the early populations was significantly shorter than the controls, while that of the late populations was significantly longer than the controls. The light-induced phase response curve of the selected populations differed significantly within groups as well as from the controls. Such modifications in the circadian phenotypes of the selected populations due to heritable changes in genetic architecture, in response to imposed selection pressure, suggest that the circadian clocks underlying emergence and locomotor activity rhythms in D. melanogaster evolve as a correlated response to selection on the timing of adult emergence.

Non-ventral lateral neuron-based, non-PDF-mediated clocks control circadian egg-laying rhythm in Drosophila melanogaster.

The authors report the results of their study aimed at investigating the consequence of targeted ablation of ventral lateral neurons (LN(v)s--neurons regulating eclosion and locomotor activity rhythms) and genetic disruption of pigment-dispersing factor (PDF--an important output of circadian clocks) on the egg-laying rhythm of Drosophila melanogaster. The results clearly suggest that genetic ablation of LN(v)s and loss of function mutation of PDF abolish eclosion and locomotor activity rhythms, whereas the egg-laying rhythm continues unabated. Furthermore, the results also demonstrate that the period of egg-laying rhythm remains unchanged under different ambient temperatures and nutrition levels, suggesting that the egg-laying rhythm of D. melanogaster is temperature and nutrition compensated. Based on these results, the authors conclude that the egg-laying rhythm in D. melanogaster is regulated by non-LN(v)-based, non-PDF-mediated circadian clocks.

Evolution of temporal order in living organisms.

Circadian clocks are believed to have evolved in parallel with the geological history of the earth, and have since been fine-tuned under selection pressures imposed by cyclic factors in the environment. These clocks regulate a wide variety of behavioral and metabolic processes in many life forms. They enhance the fitness of organisms by improving their ability to efficiently anticipate periodic events in their external environments, especially periodic changes in light, temperature and humidity. Circadian clocks provide fitness advantage even to organisms living under constant conditions, such as those prevailing in the depth of oceans or in subterranean caves, perhaps by coordinating several metabolic processes in the internal milieu. Although the issue of adaptive significance of circadian rhythms has always remained central to circadian biology research, it has never been subjected to systematic and rigorous empirical validation. A few studies carried out on free-living animals under field conditions and simulated periodic and aperiodic conditions of the laboratory suggest that circadian rhythms are of adaptive value to their owners. However, most of these studies suffer from a number of drawbacks such as lack of population-level replication, lack of true controls and lack of adequate control on the genetic composition of the populations, which in many ways limits the potential insights gained from the studies. The present review is an effort to critically discuss studies that directly or indirectly touch upon the issue of adaptive significance of circadian rhythms and highlight some shortcomings that should be avoided while designing future experiments.

Possible role of eclosion rhythm in mediating the effects of light-dark environments on pre-adult development in Drosophila melanogaster.

BACKGROUND: In insects, circadian clocks have been implicated in affecting life history traits such as pre-adult development time and adult lifespan. Studies on the period (per) mutants of Drosophila melanogaster, and laboratory-selected lines of Bactrocera cucurbitae suggested a close link between circadian clocks and development time. There is a possibility of clock genes having pleiotropic effects on clock period and pre-adult development time. In order to avoid such pleiotropic effects we have used wild type flies of same genotype under environments of different periodicities, which phenotypically either speeded up or slowed down the eclosion clock of D. melanogaster. RESULTS: We assayed pre-adult development time and pre-adult survivorship of four laboratory populations of D. melanogaster, under five different light regimes, continuous light (LL), continuous darkness (DD), and light-dark (LD) cycles of 10:10 h (T20), 12:12 h (T24), and 14:14 h (T28). Although the development time was significantly different in most light regimes, except for females under T24 &T28, pre-adult survivorship remained largely unaffected. The development time was shortest under LL, followed by T20, DD, T24 and T28 regimes, in that order. Interestingly the development time showed a positive correlation with the period of eclosion rhythm, i.e., faster oscillations were associated with faster development, and slower oscillations with slower development. CONCLUSION: Based on these results we conclude that periodicity of imposed LD cycles, and/or of eclosion rhythm plays a key role in regulating the duration of pre-adult development in D. melanogaster in a manner that does not involve direct pleiotropic effects of clock genes on both clock period and development time.

Multi-oscillatory control of eclosion and oviposition rhythms in Drosophila melanogaster: evidence from limits of entrainment studies.

The eclosion and oviposition rhythms of flies from a population of Drosophila melanogaster maintained under constant conditions of the laboratory were assayed under constant light (LL), constant darkness (DD), and light/dark (LD) cycles of 10:10h (T20), 12:12h (T24), and 14:14h (T28). The mean (+/- 95% confidence interval; CI) free-running period (tau) of the oviposition rhythm was 26.34 +/- 1.04h and 24.50 +/- 1.77h in DD and LL, respectively. The eclosion rhythm showed a tau of 23.33 +/- 0.63 h (mean +/- 95% CI) in DD, and eclosion was not rhythmic in LL. The tau of the oviposition rhythm in DD was significantly greater than that of the eclosion rhythm. The eclosion rhythm of all 10 replicate vials entrained to the three periodic light regimes, T20, T24, and T28, whereas the oviposition rhythm of only about 24 and 41% of the individuals entrained to T20 and T24 regimes, respectively, while about 74% of the individuals assayed in T28 regimes showed entrainment. Our results thus clearly indicate that the tau and the limits of entrainment of eclosion rhythm are different from those of the oviposition rhythm, and hence this reinforces the view that separate oscillators may regulate these two rhythms in D. melanogaster.

Circadian clocks and life-history related traits: is pupation height affected by circadian organization in Drosophila melanogaster?

In D. melanogaster, the observation of greater pupation height under constant darkness than under constant light has been explained by the hypothesis that light has an inhibitory effect on larval wandering behaviour, preventing larvae from crawling higher up the walls of culture vials prior to pupation. If this is the only role of light in affecting pupation height, then various light : dark regimes would be predicted to yield pupation heights intermediate between those seen in constant light and constant darkness. We tested this hypothesis by measuring pupation height under various light : dark regimes in four laboratory populations of Drosophila melanogaster. Pupation height was the greatest in constant darkness, intermediate in constant light, and the least in a light/dark regime of LD 14:14 h. The results clearly suggest that there is more to light regime effects on pupation height than mere behavioural inhibition of wandering larvae, and that circadian organization may play some role in determining pupation height, although the details of this role are not yet clear. We briefly discuss these results in the context of the possible involvement of circadian clocks in life-history evolution.

Glycogen synthase kinase 3beta as a likely target for the action of lithium on circadian clocks.

Although lithium is one of the most commonly used drugs in the prophylaxis and treatment of bipolar disorder, the mechanisms underlying its therapeutic action are still unclear. Together with its mood-stabilizing effects, lithium is also known to influence the circadian clocks of several organisms including man. Circadian rhythms are altered in patients with bipolar disorder, and it is believed that these rhythms may play an important role in disease mechanisms. It is therefore possible that some of the therapeutic actions of lithium may be related to its effect on circadian clocks. Identifying the targets for lithium's action on circadian clocks would therefore be important both for understanding the mechanisms of its therapeutic effect and also in further understanding disease mechanisms in bipolar disorders. Using Drosophila melanogaster as a model system, we show that long-term administration of lithium results in lengthening of the free-running period (tau) of circadian locomotor activity rhythm of flies in constant darkness (DD). This effect occurs at concentrations similar to the plasma levels of lithium used in the treatment of bipolar disorder. The lithium-treated flies also show reduced activity of one of the previously reported targets of lithium action, Glycogen Synthase Kinase 3beta (GSK 3beta). GSK 3beta has been shown to be involved in the regulation of circadian clocks as the down regulation of this protein results in an elongation of tau. The tau elongation resembles the effect seen with lithium administration in a number of organisms including man, and taken together with the earlier observations our results suggest that lithium inhibits the activity of GSK 3beta to produce its effect on circadian clocks.

Entrainment of eclosion rhythm in Drosophila melanogaster populations reared for more than 700 generations in constant light environment.

In this paper, we report the results of our extensive study on eclosion rhythm of four independent populations of Drosophila melanogaster that were reared in constant light (LL) environment of the laboratory for more than 700 generations. The eclosion rhythm of these flies was assayed under LL, constant darkness (DD) and three periodic light-dark (LD) cycles (T20, T24, and T28). The percentage of vials from each population that exhibited circadian rhythm of eclosion in DD and in LL (intensity of approximately 100 lux) was about 90% and 18%, respectively. The mean free-running period (tau) of eclosion rhythm in DD was 22.85 +/- 0.87 h (mean +/- SD). Eclosion rhythm of these flies entrained to all the three periodic LD cycles, and the phase relationship (psi) of the peak of eclosion with respect to "lights-on" of the LD cycle was significantly different in the three periodic light regimes (T20, T24, and T28). The results thus clearly demonstrate that these flies have preserved the ability to exhibit circadian rhythm of eclosion and the ability to entrain to a wide range of periodic LD cycles even after being in an aperiodic environment for several hundred generations. This suggests that circadian clocks may have intrinsic adaptive value accrued perhaps from coordinating internal metabolic cycles in constant conditions, and that the entrainment mechanisms of circadian clocks are possibly an integral part of the clockwork.