Reciprocal latitudinal clines in oviposition behavior ofPapilio glaucus andP. canadensis across the Great Lakes hybrid zone: possible sex-linkage of oviposition preferences (original) (raw)

Preference Variation in the Polyphagous Tiger Swallowtail Butterfly (Lepidoptera: Papilionidae)

Environmental Entomology, 1999

For polyphagous insect species, variation in oviposition preference often sets the boundaries within which host use patterns can evolve. Ultimately, host choice is a function of genetic predisposition, physiological state, and past experiences of ovipositing females. Here we explore preference variation among female tiger swallowtail butterßies, Papilio glaucus L., to investigate rank-order and speciÞcity changes caused by genetic and environmental inßuences. Hosts differed in their overall relative acceptability to ovipositing females. Preference variation among females was extensive, however, and expressed as both differences in relative Þdelity to particular hosts and differences in the host most preferred. Subsequent analysis of 2 of these hosts indicated that heritable variation among females was associated with differences in speciÞcity toward the less preferred host rather than how females ranked the hosts. Thus, preference hierarchies should be conserved among P. glaucus populations encountering different host environments. This result is consistent with patterns we reported earlier for regional P. glaucus populations. Evidence of apparent links between female preference and factors unrelated to host-choice per se suggest that host-choice behavior is labile. Patterns of egg distributions across hosts will thus not necessarily reßect adaptive responses and optimal behaviors. We discuss our Þndings with respect to adaptation and evolution of host use patterns in P. glaucus.

Absence of Behavioral Induction in Oviposition Preference of Papilio Glaucus (Lepidoptera: Papilionidae)

Great Lakes Entomologist, 1993

This study addressed the possible behavioraHnduction effects of previous exposure to several specific host plants on subsequent host "preference hierar­ chy" and "specificity" (i.e .. how far down the ranking order a female will go) in the most polyphagous swallowtail butterfly in the world, Papilio glaucus (Papilionidae). Multi-choice preference bioassays using individual females in revolving arenas were used to assess one of the potentially most significant non-genetic sources of variation: learned (or induced) oviposition preferences. Results of the 4-choice studies using tulip tree (Liriodendron tulipifera; Mag­ noliaceae), black cherry (Prunus serotina; Rosaceae), quaking aspen (Populus tremuloides; Salicaceae), and hoptree (Ptelea trifoliata; Rutaceae), fail to show any significant oviposition preference induction with two-day prior exposure to any of the host species tested. It appears that the eastern tiger swallowtail butterfly, while polyphagous as a sp...

The Benefit of Additional Oviposition Targets for a Polyphagous Butterfly

Journal of Insect Science, 2007

While the reasons for the prevalence of specialists over generalists among herbivorous insects have been at the focus of much interest, less effort has been put into understanding the polyphagous exceptions. Recent studies have suggested that these exceptions may be important for insect diversification, which calls for a better understanding of the potential factors that can lead to an increased host plant repertoire. Females of the Nymphalid butterfly, Polygonia c-album, were used to test if egg output and/or likelihood of finding a host increased with the addition of a secondary host. There was no effect of prior eggs on the host for willingness to oviposit on a plant. The main experiments were conducted both in small laboratory cages and in large outdoor experimental arenas. No positive effect was found when another oviposition target was added in small cages in the laboratory. On the other hand, in the outdoor arenas the females more often found a host to oviposit on and had a higher egg output when they had access to an additional host, even though the second host was lower in their preference hierarchy. The difference between these experiments was attributed to searching for acceptable host plants within a patch, a factor that was included in the large cages but not in the small. When host availability is limited, adding oviposition targets can potentially act to counterbalance specialization and thus favor the evolution of generalization.

Interspecific Comparison of Pupation Site Preference in Swallowtail Butterflies (Lepidoptera: Papilionidae): Implications for Evolution of Plasticity in Pupal Color

Annals of the Entomological Society of America, 2005

Variation in pupation site preference is hypothesized to drive the evolution of environmentally cued pupal color dimorphism in swallowtail butterßies. Support for this hypothesis comes from comparisons of natural pupation sites of species monomorphic and dimorphic for pupal color. Here, we show that interspeciÞc differences in pupation site preferences in nature are to a large extent mimicked in a controlled common garden experiment, suggesting that these differences are genetic. We gave larvae of three swallowtail species a choice of yellow and blue surfaces for pupation. Given the absorption spectra of green vegetation and the spectral sensitivities of the larval eyes, yellow and blue surfaces should be strong indicators of green and brown pupation sites, respectively. Papilio glaucus L., which produces only brown pupae and pupates near the ground in nature, chose to pupate near the bottom of the blue surfaces. In contrast, Battus philenor (L.) and Eurytides marcellus (Cramer), which produce dimorphic pupae, chose to pupate on both yellow and blue surfaces. B. philenor typically chose sites on blue surfaces that were signiÞcantly higher than were those of P. glaucus. We also found no differences between geographic populations of B. philenor. The distribution of pupation heights for E. marcellus was bimodal, possibly indicating a genetic polymorphism in pupation site preference. In a separate experiment, we asked whether rearing photoperiod affected pupation site preferences in Papilio polyxenes F. as suggested by observations in the Þeld. Our results showed a clear effect, with larvae choosing only brown pupation sites when reared on an autumnal photoperiod.

The Relationship Between Habitat Selection and Preference for Adult and Larval Food Resources in the Polyphagous Butterfly Vanessa cardui (Lepidoptera: Nymphalidae)

Journal of Insect Behavior, 2005

Here I focus on the potential conflict between searching for nectar plants and for larval food plants. I test if the butterfly Vanessa cardui, which can use some of its larval food plants as nectar sources, is able to rationalize this search problem by combining the two search tasks. Lab-experiments revealed a higher oviposition preference for Cirsium arvense over Urtica dioica and a corresponding difference in larval performance. Contrary to predictions, there was no effect of inflorescences on oviposition. However, experiments in large outdoor cages showed a higher occupancy and a higher level of oviposition in patches with access to nectar sources, even on U. dioica. Hence, while there was no preference for individual plants with flowers, the results suggests that V. cardui is simplifying its search task to primarily search for hosts in nectar-rich patches. This strategy allows females to increase oviposition rate, but it is likely that it comes at the expense of not always using optimal host plants in terms of offspring performance.

Butterfly oviposition preference is not related to larval performance on a polyploid herb

Ecology and Evolution

The preference-performance hypothesis predicts that female insects maximize their fitness by utilizing host plants which are associated with high larval performance. Still, studies with several insect species have failed to find a positive correlation between oviposition preference and larval performance. In the present study, we experimentally investigated the relationship between oviposition preferences and larval performance in the butterfly Anthocharis cardamines. Preferences were assessed using both cage experiments and field data on the proportion of host plant individuals utilized in natural populations. Larval performance was experimentally investigated using larvae descending from 419 oviposition events by 21 females on plants from 51 populations of two ploidy types of the perennial herb Cardamine pratensis. Neither ploidy type nor population identity influenced egg survival or larval development, but increased plant inflorescence size resulted in a larger final larval size. There was no correlation between female oviposition preference and egg survival or larval development under controlled conditions. Moreover, variation in larval performance among populations under controlled conditions was not correlated with the proportion of host plants utilized in the field. Lastly, first instar larvae added to plants rejected for oviposition by butterfly females during the preference experiment performed equally well as larvae growing on plants chosen for oviposition. The lack of a correlation between larval performance and oviposition preference for A. cardamines under both experimental and natural settings suggests that female host choice does not maximize the fitness of the individual offspring.

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Allochronic isolation and incipient hybrid speciation in tiger swallowtail butterflies

Oecologia, 2010

Hybridization leading to reproductively isolated, novel genotypes is poorly understood as a means of speciation and few empirical examples have been studied. In 1999, a previously non-existent delayed Xight of what appeared to be the Canadian tiger swallowtail butterXy, Papilio canadensis, was observed in the Battenkill River Valley, USA. Allozyme frequencies and morphology suggest that this delayed Xight was the product of hybridization between Papilio canadensis and its sibling species Papilio glaucus. The mitochondrial DNA (mtDNA) restriction fragment length polymorphisms presented here indicate that only P. canadensis-like mtDNA occurs in this population, suggesting that introgression likely occurred from hybrid males mating with P. canadensis females. Preliminary studies of this population indicated that delayed post-diapause pupal emergence in this hybrid genotype was the root cause behind the observed delayed Xight, which suggests a potential empirical example of a mechanism leading to reproductive isolation. Here we provide further evidence of the role of adult pupal emergence as a reproductive barrier likely leading to reproductive isolation. In particular, we present results from pupal emergence studies using four diVerent spring and two diVerent winter temperature treatments. The results indicate a clear separation of adult emergences between the hybrid population and both parental species. However, our results indicate that exceptionally hot springs are likely to lead to greater potential for overlap between the local parental species, P. canadensis, and this delayed population with hybrid origins. Conversely, our results also show that warmer winters are likely to increase the temporal separation of the hybrid population and the parental species. Finally, we report recently collected evidence that this hybrid population remains morphologically distinct.

Discordant Divergence Times Among Z-Chromosome Regions Between Two Ecologically Distinct Swallowtail Butterfly Species

Evolution, 2007

We investigate multilocus patterns of differentiation between parental populations of two swallowtail butterfly species that differ at a number of ecologically important sex-linked traits. Using a new coalescent-based approach, we show that there is significant heterogeneity in estimated divergence times among five Z-linked markers, rejecting a purely allopatric speciation model. We infer that the Z chromosome is a mosaic of regions that differ in the extent of historical gene flow, potentially due to isolating barriers that prevent the introgression of species-specific traits that result in hybrid incompatibilities. Surprisingly, a candidate region for a strong barrier to introgression, Ldh, does not show a significantly deeper divergence time than other markers on the Z chromosome.

Recent hybrids recapitulate ancient hybrid outcomes

Genomic outcomes of hybridization depend on selection and recombination in hybrids. Whether these processes have similar effects on hybrid genome composition in contemporary hybrid zones versus ancient, stabilized hybrid lineages is unknown. Here we show that patterns of introgression in a contemporary hybrid zone in Lycaeides butterflies predict patterns of ancestry in geographically adjacent, ancient hybrid populations. We find a particularly striking lack of ancestry from one of the hybridizing taxa, Lycaeides melissa, on the Z chromosome in both the ancient and contemporary hybrids. The same pattern of reduced L. melissa ancestry on the Z chromosome is seen in two other ancient hybrid lineages. More generally, we find that patterns of ancestry in ancient hybrids are remarkably predictable from contemporary hybrids, which suggests selection affects hybrid genomes in a similar way across disparate time scales and during distinct stages of speciation and species breakdown

Host-associated genetic differentiation in a seed parasitic weevil Rhinusa antirrhini (Coleptera: Curculionidae) revealed by mitochondrial and nuclear sequence data

Molecular Ecology, 2010

Plant feeding insects and the plants they feed upon represent an ecological association that is thought to be a key factor for the diversification of many plant feeding insects, through differential adaptation to different plant selective pressures. While a number of studies have investigated diversification of plant feeding insects above the species level, relatively less attention has been given to patterns of diversification within species, particularly those that also require plants for oviposition and subsequent larval development. In the case of plant feeding insects that also require plant tissues for the completion of their reproductive cycle through larval development, the divergent selective pressure not only acts on adults, but on the full life history of the insect. Here we focus attention on Rhinusa antirrhini (Curculionidae), a species of weevil broadly distributed across Europe that both feeds on, and oviposits and develops within, species of the plant genus Linaria (Plantaginaceae). Using a combination of mtDNA (COII) and nuclear DNA (EF1-a) sequencing and copulation experiments we assess evidence for host associated genetic differentiation within R. antirrhini. We find substantial genetic variation within this species that is best explained by ecological specialisation on different host plant taxa. This genetic differentiation is most pronounced in the mtDNA marker, with patterns of genetic variation at the nuclear marker suggesting incomplete lineage sorting and ⁄ or gene flow between different host plant forms of R. antirrhini, whose origin is estimated to date to the mid-Pliocene (3.77 Mya; 2.91-4.80 Mya).

Genotypic and Environmental Effects on Flight Activity and Oviposition in the Glanville Fritillary Butterfly

American Naturalist, 2008

Adverse environmental conditions constrain active flight and thereby limit reproduction in most insects. Butterflies have evolved various adaptations in order to thermoregulate, allowing females to search for nectar and to oviposit under unfavorable thermal conditions. We studied experimentally and with observational data the effect of low ambient temperatures experienced in the morning on the timing of oviposition and clutch size in the Glanville fritillary butterfly (Melitaea cinxia). Comparisons were made between individuals with different forms of the gene Pgi, encoding the glycolytic enzyme phosphoglucose isomerase, since naturally segregating variation at Pgi is known to be correlated with flight metabolic rate, flight performance, and fecundity. Experiencing low temperature in the morning delayed the initiation of oviposition and decreased clutch size. We used a thermal image camera to measure the thoracic surface temperature of butterflies immediately after voluntary flight. Single nucleotide polymorphism at Pgi was associated with thoracic temperature at low ambient temperatures. This has consequences for reproduction because females that are able to fly at lower ambient temperatures generally initiate oviposition earlier in the afternoon, when the environmental conditions are most favorable and the average egg clutch size is generally largest. These results suggest that variation in physiological and molecular capacity to sustain active flight at low ambient temperature has significant fitness-related consequences in insects.

Gene Flow Between Great Lakes Region Populations of the Canadian Tiger Swallowtail Butterfly, Papilio Canadensis, Near the Hybrid Zone With P. Glaucus (Lepidoptera: Papilionidae)

The Great Lakes Entomologist

Papilio canadensis were sampled from three locations on either side of Lake Michigan to study gene flow near and through a butterfly hybrid zone. Allele frequencies at four polymorphic enzyme loci, as indicated by allozyme electrophoresis, were similar in all samples. Values for F ST were close to zero, indicating that gene flow is high among these populations, even when separated by Lake Michigan. We developed a mitochondrial DNA marker with diagnostic differences between P. canadensis and its parapatric sister species Papilio glaucus, based on PCR-RFLP. P. glaucus haplotypes of this mtDNA marker and P. glaucus alleles of a diagnostic allozyme locus (PGD) were found in P. canadensis populations sampled in Michigan's Lower Peninsula but not in the Upper Peninsula or Northern Minnesota. The presence of P. glaucus alleles in P. canadensis populations could be due to introgression through hybridization, or could be remnants of a P. glaucus population that was inundated by an influx of P. canadensis alleles.

Local Enhancement in Mud-Puddling Swallowtail Butterflies ( Battus philenor and Papilio glaucus

Journal of Insect Behavior, 2006

Male butterflies aggregate at moist soil to acquire nutrients, a phenomenon termed “mud-puddling.” We studied the attraction of free-flying Papilio glaucus and Battus philenor swallowtails to dead decoys of those two species at artificial puddles moistened with NaCl solution. Both species landed preferentially at puddles with a decoy present rather than at unbaited puddles, demonstrating very strong local enhancement, a form of social facilitation. Papilio glaucus were attracted only to intraspecific decoys, whereas Battus philenor exhibited both intraspecific and interspecific attraction. Circular discs cut from the hindwings of male Battus were highly attractive to male Battus but completely unattractive to Papilio glaucus. The visual cues attractive to males in their search for salts differ between these two swallowtail species for unexplained reasons.

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