Closely related sympatric species are expected to evolve strong species discrimination because of the reinforcement of mate preferences. Fitness costs of heterospecific matings are thought to be higher in females than in males, and females are therefore expected to show stronger species discrimination than males. Here, we investigated gender and species differences in sexual isolation in a sympatric species pair of Calopteryx damselflies. The genus Calopteryx is one of the classic examples of reproductive character displacement in evolutionary biology, with exaggerated interspecific differences in the amount of dark wing coloration when species become sympatric. Experimental manipulation of the extent of dark wing coloration revealed that sexual isolation results from both female and male mate discrimination and that wing melanization functions as a species recognition character. Female choice of conspecific males is entirely based on wing coloration, whereas males in one species also use other species recognition cues in addition to wing color. Stronger species discrimination ability in males is presumably an evolutionary response to an elevated male predation risk caused by conspicuous wing coloration. Gender differences in species discrimination and fitness costs of male courtship can thus shed new light on the evolution of asymmetric sexual isolation and the reinforcement of mate preferences.
Characterizing and quantifying genome size variation among organisms and understanding if genome size evolves as a consequence of adaptive or stochastic processes have been long-standing goals in evolutionary biology. Here, we investigate genome size variation and association with transposable elements (TEs) across lepidopteran lineages using a novel genome assembly of the common wood-white (Leptidea sinapis) and population re-sequencing data from both L. sinapis and the closely related L. reali and L. juvernica together with 12 previously available lepidopteran genome assemblies. A phylogenetic analysis confirms established relationships among species, but identifies previously unknown intraspecific structure within Leptidea lineages. The genome assembly of L. sinapis is one of the largest of any lepidopteran taxon so far (643 Mb) and genome size is correlated with abundance of TEs, both in Lepidoptera in general and within Leptidea where L. juvernica from Kazakhstan has considerably larger genome size than any other Leptidea population. Specific TE subclasses have been active in different Lepidoptera lineages with a pronounced expansion of predominantly LINEs, DNA elements, and unclassified TEs in the Leptidea lineage after the split from other Pieridae. The rate of genome expansion in Leptidea in general has been in the range of four Mb/Million year (My), with an increase in a particular L. juvernica population to 72 Mb/My. The considerable differences in accumulation rates of specific TE classes in different lineages indicate that TE activity plays a major role in genome size evolution in butterflies and moths.
Although predation is thought to affect species divergence, the effects of predator-mediated natural selection on species divergence and in nonadaptive radiations have seldom been studied. Wing melanization in Calopteryx damselflies has important functions in sexual selection and interspecific interactions and in species recognition. The genus Calopteryx and other damselfly genera have also been put forward as examples of radiations driven by sexual selection. We show that avian predation strongly affects natural selection on wing morphology and male wing melanization in two congeneric and sympatric species of this genus (Calopteryx splendens and Calopteryx virgo). Predation risk was almost three times higher for C. virgo, which has an exaggerated degree of wing melanization, than it was for the less exaggerated, sympatric congener C. splendens. Selective predation on the exaggerated species C. virgo favored a reduction and redistribution of the wing melanin patch. There was evidence for nonlinear selection involving wing patch size, wing patch darkness, and wing length and width in C. splendens but weaker nonlinear selection on the same trait combinations in C. virgo. Selective predation could interfere with species divergence by sexual selection and may thus indirectly affect male interspecific interactions, reproductive isolation, and species coexistence in this genus.
The relative strength of different types of directional selection has seldom been compared directly in natural populations. A recent meta-analysis of phenotypic selection studies in natural populations suggested that directional sexual selection may be stronger in magnitude than directional natural selection, although this pattern may have partly been confounded by the different time scales over which selection was estimated. Knowledge about the strength of different types of selection is of general interest for understanding how selective forces affect adaptive population divergence and how they may influence speciation. We studied divergent selection on morphology in parapatric, natural damselfly (Calopteryx splendens) populations. Sexual selection was stronger than natural selection measured on the same traits, irrespective of the time scale over which sexual selection was measured. Visualization of the fitness surfaces indicated that population divergence in overall morphology is more strongly influenced by divergent sexual selection rather than natural selection. Courtship success of experimental immigrant males was lower than that of resident males, indicating incipient sexual isolation between these populations. We conclude that current and strong sexual selection promotes adaptive population divergence in this species and that premating sexual isolation may have arisen as a correlated response to divergent sexual selection. Our results highlight the importance of sexual selection, rather than natural selection in the adaptive radiation of odonates, and supports previous suggestions that divergent sexual selection promotes speciation in this group.
The majority of phytophagous insects are relatively specialized in their food habits, and specialization in resource use is expected to be favored by selection in most scenarios. Ecological generalization is less common and less well understood, but it should be selected for by (1) rarity of resources, (2) resource inconstancy, or (3) unreliability of resource quality. Here, we test these predictions by studying egg distribution and offspring survival in the orange tip butterfly, Anthocharis cardamines, on different host plants in Sweden over a five-year period. A total of 3800 eggs were laid on 16 of the 18 crucifers available at the field site during the five years. Three main factors explained host plant generalization: (1) a rarity of food resources in which the female encounter rate of individual crucifer plants was low and within-year phenological succession of flowering periods of the different crucifers meant that individual species were suitable for oviposition only within a short time window, which translates to a low effective abundance of individual crucifer species as experienced by females searching for host plants, making specialization on a single crucifer species unprofitable; (2) variation in food resources in which among-year variation in availability of any one host plant species was high; and (3) larval survivorship varied unpredictably among years on all host plants, thereby necessitating a bet-hedging strategy and use of several different host plants. Unpredictable larval survival was caused by variation in plant stand habitat characteristics, which meant that drowning and death from starvation affected different crucifers differently, and by parasitism, which varied by host plant and year. Hence, our findings are in agreement with the theoretical explanation of ecological generalization above, helping to explain why A. cardamines is a generalist throughout its range with respect to genera within the Cruciferae.
Molecular studies of natural populations are often designed to detect and categorize hidden layers of cryptic diversity, and an emerging pattern suggests that cryptic species are more common and more widely distributed than previously thought. However, these studies are often decoupled from ecological and behavioural studies of species divergence. Thus, the mechanisms by which the cryptic diversity is distributed and maintained across large spatial scales are often unknown. In 1988, it was discovered that the common Eurasian Wood White butterfly consisted of two species (Leptidea sinapis and Leptidea reali), and the pair became an emerging model for the study of speciation and chromosomal evolution. In 2011, the existence of a third cryptic species (Leptidea juvernica) was proposed. This unexpected discovery raises questions about the mechanisms preventing gene flow and about the potential existence of additional species hidden in the complex. Here, we compare patterns of genetic divergence across western Eurasia in an extensive data set of mitochondrial and nuclear DNA sequences with behavioural data on inter- and intraspecific reproductive isolation in courtship experiments. We show that three species exist in accordance with both the phylogenetic and biological species concepts and that additional hidden diversity is unlikely to occur in Europe. The Leptidea species are now the best studied cryptic complex of butterflies in Europe and a promising model system for understanding the formation of cryptic species and the roles of local processes, colonization patterns and heterospecific interactions for ecological and evolutionary divergence.
We investigate the niche separation in space and time between the Palearctic sister species Leptidea sinapis and L. reali (Lepidoptera, Pieridae) in central Sweden. Using field sampling, we show that L. reali is a habitat specialist confined to meadows, whereas L. sinapis is a habitat generalist also inhabiting forests. This difference in habitat utilization was corroborated by experimental release of laboratory-reared L. sinapis and L. reali in two adjacent forest and meadow habitats during their natural flight period; virtually all recaptured L. reali that were released in the forest were later caught in the meadow, whereas L. sinapis shifted equally often from meadow to forest as in the opposite direction. In the field, both species fly in May-June, but L. reali appears on average a week earlier in spring and has a substantial second generation in July, whereas L. sinapis is practically univoltine. When overwintered pupae were incubated under identical conditions in the laboratory, females did, however, not differ in phenology, and L. sinapis males actually emerged earlier than L. reali males. When larvae were reared at 23°C on the host plant Lotus corniculatus at a range of daylengths, both species produced a substantial proportion of directly developing individuals at an 18.5 h daylength or longer. When reared at 23°C and a 22 h daylength, L. reali showed an overall higher propensity to develop directly than L. sinapis on plant species originating from both the meadow and the forest habitat. Both Leptidea species showed a lower propensity to enter direct development on forest associated plants than on meadow associated plants. Hence, we suggest that the difference in phenology and voltinism between
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