The paradox of successful invading species is that they are likely to be genetically depauperate compared to their source population. This study on Colorado potato beetles is one of the few studies of the genetic consequences of continent-scale invasion in an insect pest. Understanding gene flow, population structure and the potential for rapid evolution in native and invasive populations offers insights both into the dynamics of small populations that become successful invaders and for their management as pests. We used this approach to investigate the invasion of the Colorado potato beetle (Leptinotarsa decemlineata) from North America to Europe. The beetles invaded Europe at the beginning of the 20th century and expanded almost throughout the continent in about 30 years. From the analysis of mitochondrial DNA (mtDNA) and amplified fragment length polymorphism (AFLP) markers, we found the highest genetic diversity in beetle populations from the central United States. The European populations clearly contained only a fraction of the genetic variability observed in North American populations. European populations show a significant reduction at nuclear markers (AFLPs) and are fixed for one mitochondrial haplotype, suggesting a single successful founder event. Despite the high vagility of the species and the reduction of genetic diversity in Europe, we found a similar, high level of population structure and low gene flow among populations on both continents. Founder events during range expansion, agricultural management with crop rotation, and selection due to insecticide applications are most likely the causes partitioning genetic diversity in this species.
The butterfly Bicyclus anynana exhibits phenotypic plasticity involving the wet-season phenotype, which possesses marginal eyespots on the ventral surface of the wings, and the dry-season form, which lacks these eyespots. We examined the adaptive value of phenotypic plasticity of B. anynana in relation to the defence mechanisms of crypsis and deflection. We assessed the visibility differences between spotless and spotted butterflies against backgrounds of brown (dry season) or green (wet season) leaves. Spotless butterflies were highly cryptic and less predated by adult bird predators than were spotted ones when presented against brown leaf litter. However, the advantage of crypsis disappeared in the wet-season habitat as both forms were equally visible. In later experiments, naive birds presented with resting butterflies in the wet-season habitat tended to learn more rapidly to capture spotless butterflies, suggesting a slight selective advantage of possessing eyespots. Moreover, marginal eyespots increased significantly the escape probability of butterflies that were attacked by naive birds compared to those attacked by adult birds, although there were no differences in prey capture success within naive predators. Our results show that natural selection acts against eyespots in the dry season, favouring crypsis, whereas in the wet season it may favour eyespots as deflective patterns.
We studied selection by predators for cryptic prey coloration in a visually heterogeneous habitat that consists of two microhabitats. It has been suggested that the probability of escaping detection in such habitats might be optimized by maximizing crypsis in one of the microhabitats. However, a recent model indicates that a coloration that compromises the requirements of di¡erent microhabitats might sometimes be the optimal solution. To experimentally study these hypotheses, we allowed great tits (Parus major L.) to search for arti¢cial prey items in two di¡erent microhabitats (background boards): small patterned and large patterned. On each board there was one prey item that was either small-patterned, large-patterned or medium-patterned and thus compromised. Search time was used as the measure of crypsis and was on average longer on the large-patterned than on the small-patterned background. On the small-patterned background, the small-patterned prey was more cryptic than the compromised prey, which was in turn more cryptic than the large-patterned prey. On the large-patterned background, the small-patterned prey was least cryptic, but the compromised prey did not di¡er signi¢cantly from the large-patterned prey. The compromised coloration had lower predation risk than the matching colorations. This indicates that in some conditions a compromised coloration might be the best strategy for the prey and has important implications for the study of animal coloration.
The evolution of aposematism, a phenomenon where prey species conspicuously advertise their unprofitability to predators, is puzzling. How did conspicuousness evolve, if it simultaneously increased the likelihood of an inexperienced predator to detect the prey and presumably kill it? Antiapostatic selection, where rare prey is predated relatively more often, is considered as another major difficulty for aposematism to evolve. However, the risk of being conspicuous in low frequencies has not been experimentally tested. We designed an experiment to test how frequency (4%, 12%, 32%) of conspicuous aposematic prey and its dispersion type (solitary vs. aggregated) affect an initial predation risk of the prey and in avoidance learning of predators. Wild great tits (Parus major) were predators on artificial prey in a ''novel world.'' The relative mortality of aposematic prey was antiapostatic, thus the frequency-dependent predation was most severe at low frequencies. In all frequencies, aggregated aposematic prey survived better than solitary prey. Surprisingly, learning was not determined by a fixed number of unpalatable prey eaten, but at low frequencies fewer aposematic individuals eaten generated predators' avoidance learning. However, per-capita risk for the prey remained highest at low frequencies. Our results underscore the problems of initial evolution of rare conspicuous morphs. Aggregated prey suffered less from predation, indicating selective advantage of aggregation over solitary living for a conspicuous individual.
Many butterfly genera are characterised by the presence of marginal eyespots on their wings. One hypothesis to account for an occurrence of eyespots is that these wing pattern elements are partly the outcome of visual selection by predators. Bicyclus anynana (Satyrinae) has underside spotting on its wings but there is also a seasonal form in which the eyespots are reduced in size or totally absent. This natural variation gives us a useful tool to test the hypothesis that marginal eyespot patterns can decoy the attacking predator by, at least sometimes, diverting attack from vital body parts to the edges of the wings. We used lizards, Anolis carolinensis, and pied flycatchers, Ficedula hypoleuca, as predators for living spotted and spotless B. anynana. The presence of eyespots did not increase the escape probability of resting butterflies once captured (even a form with enlarged eyespots did not add to effective deflection of attacks). There was also no evidence that eyespots influenced the location of strikes by the predators. This study thus provides no support that marginal eyespot patterns can act as an effective deflection mechanism to avoid lizard or avian predation.
Müllerian mimicry, where unpalatable prey share common warning patterns, has long fascinated evolutionary biologists. It is commonly assumed that Müllerian mimics benefit by sharing the costs of predator education, thus reducing per capita mortality, although there has been no direct test of this assumption. Here, we specifically measure the selection pressure exerted by avian predators on unpalatable prey with different degrees of visual similarity in their warning patterns. Using wild-caught birds foraging on novel patterned prey in the laboratory, we unexpectedly found that pattern similarity did not increase the speed of avoidance learning, and even dissimilar mimics shared the education of naive predators. This was a consistent finding across two different densities of unpalatable prey, although mortalities were lower at the higher density as expected. Interestingly, the mortalities of Müllerian mimics were affected by pattern similarity in the predicted way by the end of our experiment, although the result was not quite significant. This suggests that the benefits to Müllerian mimics may emerge only later in the learning process, and that predator experience of the patterns may affect the degree to which pattern similarity is important. This highlights the need to measure the behaviour of real predators if we are to understand fully the evolution of mimicry systems.
Summary 1.As organisms expand their range towards northern latitudes they will encounter selective factors like harsh winter conditions. The ability to cope with and adapt to harsh winters may depend on the variability and evolutionary potential of relevant traits. 2. One adaptation in insects is winter diapause. It is characterized by changes in physiology, behaviour or in both. Physiological changes include lowered metabolic rate that enhances survival by saving limited energy reserves during overwintering. Active behavioural changes like burrowing into the soil allow individuals to escape harsh conditions. 3. We examined variation in overwintering body mass, resting metabolic rate (CO 2 production) and diapause behaviour (burrowing into the soil), and their effects on overwintering success in the adult Colorado potato beetles (Leptinotarsa decemlineata). We conducted a full-sib ⁄ half-sib rearing experiment to estimate the evolutionary potential (heritability) of these traits. 4. High overwintering body mass and low metabolic rate were phenotypically associated with high diapause propensity (i.e. burrowing), which was linked to high overwintering survival. We found that once beetles had entered the soil, only large body mass of males was associated with high overwintering survival. However, the heritability estimates in all traits examined were low. 5. Our results show that winter conditions impose selection on diapause behaviour, which was linked to lower metabolic rate and larger body mass. If range expansion to higher latitudes requires adaptive genetic changes in diapause behaviour, metabolism, or body mass, the insufficient genetic variation in these traits suggest that the Colorado potato beetle's future potential to respond to selection due to harsher winters could be limited and thus, its range expansion could be hindered. Both physiological and behavioural adaptations are important to consider when assessing range expansion potential.
Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.
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