Migration in butterflies: a global overview.

Insect populations including butterflies are declining worldwide, and they are becoming an urgent conservation priority in many regions. Understanding which butterfly species migrate is critical to planning for their conservation, because management actions for migrants need to be coordinated across time and space. Yet, while migration appears to be widespread among butterflies, its prevalence, as well as its taxonomic and geographic distribution are poorly understood. The study of insect migration is hampered by their small size and the difficulty of tracking individuals over long distances. Here we review the literature on migration in butterflies, one of the best-known insect groups. We find that nearly 600 butterfly species show evidence of migratory movements. Indeed, the rate of 'discovery' of migratory movements in butterflies suggests that many more species might in fact be migratory. Butterfly migration occurs across all families, in tropical as well as temperate taxa; Nymphalidae has more migratory species than any other family (275 species), and Pieridae has the highest proportion of migrants (13%; 133 species). Some 13 lines of evidence have been used to ascribe migration status in the literature, but only a single line of evidence is available for 92% of the migratory species identified, with four or more lines of evidence available for only 10 species - all from the Pieridae and Nymphalidae. Migratory butterflies occur worldwide, although the geographic distribution of migration in butterflies is poorly resolved, with most data so far coming from Europe, USA, and Australia. Migration is much more widespread in butterflies than previously realised - extending far beyond the well-known examples of the monarch Danaus plexippus and the painted lady Vanessa cardui - and actions to conserve butterflies and insects in general must account for the spatial dependencies introduced by migratory movements.

Two centuries of monarch butterfly collections reveal contrasting effects of range expansion and migration loss on wing traits.

Migratory animals exhibit traits that allow them to exploit seasonally variable habitats. In environments where migration is no longer beneficial, such as oceanic islands, migration-association traits may be selected against or be under relaxed selection. Monarch butterflies are best known for their continent-scale migration in North America but have repeatedly become established as nonmigrants in the tropical Americas and on Atlantic and Pacific Islands. These replicated nonmigratory populations provide natural laboratories for understanding the rate of evolution of migration-associated traits. We measured >6,000 museum specimens of monarch butterflies collected from 1856 to the present as well as contemporary wild-caught monarchs from around the world. We determined 1) how wing morphology varies across the monarch's global range, 2) whether initial long-distance founders were particularly suited for migration, and 3) whether recently established nonmigrants show evidence for contemporary phenotypic evolution. We further reared >1,000 monarchs from six populations around the world under controlled conditions and measured migration-associated traits. Historical specimens show that 1) initial founders are well suited for long-distance movement and 2) loss of seasonal migration is associated with reductions in forewing size and elongation. Monarch butterflies raised in a common garden from four derived nonmigratory populations exhibit genetically based reductions in forewing size, consistent with a previous study. Our findings provide a compelling example of how migration-associated traits may be favored during the early stages of range expansion, and also the rate of reductions in those same traits upon loss of migration.

And the beak shall inherit - evolution in response to invasion.

The increased demographic performance of biological invaders may often depend on their escape from specifically adapted enemies. Here we report that native taxa in colonized regions may swiftly evolve to exploit such emancipated exotic species because of selection caused by invaders. A native Australian true bug has expanded it host range to include a vine imported from tropical America that has become a serious environmental weed. Based on field comparisons and historical museum specimens, we show that over the past 30-40 years, seed feeding soapberry bugs have evolved 5-10% longer mouthparts, better suited to attack the forest-invading balloon vines, which have large fruits. Laboratory experiments show that these differences are genetically based, and result in a near-doubling of the rate at which seeds are attacked. Thus a native biota that initially permits invasion may rapidly respond in ways that ultimately facilitate control.

Rapid appearance of epistasis during adaptive divergence following colonization.

Theory predicts that short-term adaptation within populations depends on additive (A) genetic effects, while gene-gene interactions 'epistasis (E)' are important only in long-term evolution. However, few data exist on the genetic architecture of adaptive variation, and the relative importance of A versus non-additive genetic effects continues to be a central controversy of evolutionary biology after more than 70 years of debate. To examine this issue directly, we conducted hybridization experiments between two populations of wild soapberry bugs that have strongly differentiated in 100 or fewer generations following a host plant shift. Contrary to expectation, we found that between-population E and dominance (D) have appeared quickly in the evolution of new phenotypes. Rather than thousands of generations, adaptive gene differences between populations have evolved in tens. Such complex genetic variation could underlie the seemingly extreme rates of evolution that are increasingly reported in many taxa. In the case of the soapberry bug, extraordinary ecological opportunity, rather than mortality, may have created hard selection for genetic variants. Because ultimate division of populations into genetic species depends on epistatic loss of hybrid compatibility, local adaptation based on E may accelerate macro-evolutionary diversification.

GENETIC DIFFERENTIATION OF FITNESS-ASSOCIATED TRAITS AMONG RAPIDLY EVOLVING POPULATIONS OF THE SOAPBERRY BUG.

In this study we used reciprocal rearing experiments to test the hypothesis that there is a genetic basis for the adaptive differences in host-use traits among host-associated soapberry bug populations (described in Carroll and Boyd 1992). These experiments were conducted on two host races from Florida, in which differences in beak length and development were found between natural populations on a native host plant species and those on a recently introduced plant species (colonized mainly post-1950). Performance was generally superior on the host species from which each lab population originated (i.e., on the "Home" host species): in analysis of variance, there was significant population-by-host interaction for size, development time, and growth rate. These results indicate that the population differences in nature are evolved rather than host induced. Increased performance on the introduced host was accompanied by reduced performance on the native host, a pattern that could theoretically promote further differentiation between the host races.

Geographic variation in embryonic development time and stage of diapause in a grasshopper.

Embryonic development times and the stage at which embryonic diapause occurs varied dramatically among 23 populations of the Melanoplus sanguinipes/ devastator species complex in California, USA. Grasshoppers were collected from a wide range of latitudes (32°57N to 41°20N) and altitudes (10m to 3031 m), spanning much of the variation in climatic conditions experienced by these insects in California. When reared in a "common garden" in the laboratory, total embryonic development times were positively correlated to the mean annual temperature of the habitat from which the grasshoppers were collected (varying from about 19 days to 32 days when reared at 27°C). These grasshoppers overwinter as diapausing eggs and the proportion of embryonic development completed prior to diapause was significantly higher in populations collected from cool habitats (>70%) than in populations collected from warm environments (<26%). The length of pre-diapause development time is determined by the stage of embryonic development at which diapause occurs, and varies considerably among populations of these grasshoppers; grasshoppers from warmer environments tend to diapause at very early stages of embryogenesis, while grasshoppers from cooler environments diapause at very late stages. The combined effect of variation in embryonic development times and variation in the stage at which diapause occurs results in a dramatic reduction in the time needed to hatch in the spring; populations from warm environments required up to 20 days (at 27°C) to hatch while populations from cool environments required as few as 5 days to complete embryonic development prior to hatching. Egg size also varied significantly among populations, but tended to be larger in populations with shorter embryonic development times. Significant family effects were observed for development time and stage of diapause, suggesting significant heritabilities for these traits, although maternal effects may also contribute to family level variation. We interpret these findings to support the hypothesis that embryonic development time and the stage of embryonic diapause have evolved as adaptations to prevailing season lengths in the study populations.

Altitudinal variation in life cycle syndromes of California populations of the grasshopper, Melanoplus sanguinipes (F.).

Life cycles of California populations of the grasshopper, Melanoplus sanguinipes, varied along an altitudinal gradient. Temperature records indicate a longer season at low altitude on the coast, based on computation of degree days available for development, even though summer air temperatures are cooler than at high altitude; this is a result of warm soil temperatures. At high and low altitudes there was a high proportion of diapause eggs oviposited, while intermediate proportions of diapause eggs occurred at mid altitudes. The low altitude, and especially sea level, populations diapaused at all stages of embryonic development, while at high altitudes most diapause occurred in the late stages just before hatch. Diapause was more intense at high altitudes. One result of diapause differences was delayed hatching in the sea level population. Nymphal development and development of adults to age at first reproduction were both accelerated at high altitude relative to sea level. At lower temperatures (27° C) there was a tendency for short days to accelerate development of sea level nymphs, but not high altitude nymphs. In both sea level and high altitude grasshoppers, short days accelerated maturation of adults to onset of oviposition at warm temperature (33° C); there was little reproduction at 27° C. Population differences for all traits studied appear to be largely genetic with some maternal effects possible. We interpret diapause variation at low and mid altitudes to be responses to environmental uncertainty and variations in development rates to be adaptations to prevailing season lengths.

Effects of freshwater and marine overwintering environments on life histories of threespine sticklebacks: evidence for adaptive variation between anadromous and resident freshwater populations.

Life history theory predicts that migratory fishes should delay reproduction, be larger at first reproduction, and have higher fecundities than nonmigrants. We tested this hypothesis by comparing life histories of anadromous ("estuary") and resident freshwater ("upstream") threespine sticklebacks (Gasterosteus aculeatus L.) from the Navarro River, California, USA. Using a split-brood, two-environment breeding design, families from cach population were divided and reared in both freshwater and seawater overwintering environments. In both treatments, the more migratory estuary sticklebacks were larger at first reproduction and had large initial clutch sizes; in the freshwater treatment, the estuary sticklebacks matured later than the upstream fish. Population means varied little across treatments, indicating that the average effects of the different overwintering conditions were slight. The responses of individual families to a given overwintering treatment were highly variable in both populations, as reflected in significant family x treatment effects for all traits. Phenotypic correlations among life history traits were significant and positive for most traits, and were similar in magnitude in both populations. Differences in the relative degree of specialization for migration may in part explain variation in life history between these populations.

RESPONSES TO SELECTION AMONG LIFE-HISTORY TRAITS IN A NONMIGRATORY POPULATION OF MILKWEED BUGS (ONCOPELTUS FASCIATUS).

Genetic parameters were assessed in the nonmigratory Puerto Rico population of the milkweed bug, Oncopeltus fasciatus, and compared with parameters estimated in a migratory population from Iowa (Palmer and Dingle, 1986). Offspring-parent regression analysis provided initial estimates of heritabilities and phenotypic and genetic correlations among wing length, head-capsule width, female age at first reproduction, fecundity for the first and second five days of reproduction by females, and clutch size for the first and second five days of reproduction by females. Replicated bidirectional selection for wing length was then imposed, with a direct response to selection revealing substantial additive genetic variance for this trait, as was also the case with the Iowa population. Assays for correlated response to selection yielded two further similarities to Iowa: a positive response in head-capsule width and no consistent response in age at first reproduction. In contrast to the results with Iowa bugs, neither regression analysis nor selection revealed statistically significant genetic correlations between fecundity measures and those of other traits. In both populations the potential exists for body-size characters to evolve together independently of age at first reproduction; but in the nonmigratory Puerto Rico bugs, fecundity does not contribute to a life-history syndrome involving genetic correlations among these traits.

Geographic variation in the effects of temperature on life-history traits in the large milkweed bug Oncopeltus fasciatus.

Complete sets of life-history data (sufficient to construct life-tables and calculate intrinsic rates of increase) were collected at each of three constant temperatures for descendants of two tropical populations of the Large Milkweed Bug, Oncopeltus fasciatus. Although the two populations occur only about 60 km apart, they experience quite different thermal regimes, with little variation in mean monthly temperature at either site. In addition to the pronounced effect of ambient temperature on life-history traits, significant population-by-temperature interactions were observed for six of the eight traits examined. The data and the recent history of the species' distribution are consistent with the hypothesis that natural selection in the cool habitat has favored improved survival and increased reproduction at cool temperatures, with some trade-offs with respect to performance at higher (but ecologically relevant) temperatures.

DIRECT AND CORRELATED RESPONSES TO SELECTION AMONG LIFE-HISTORY TRAITS IN MILKWEED BUGS (ONCOPELTUS FASCIATUS).

Offspring-parent regressions provided initial estimates of heritabilities and genetic correlations among wing length, body length, pronotum width, head-capsule width, development time, age at first reproduction, and fecundity in an Iowa population of the large milkweed bug, Oncopeltus fasciatus. Replicated, bidirectional selection for wing length was imposed for nine generations. The direct response to selection revealed the existence of substantial additive genetic variance for wing length in this population. Traits were assayed for correlated responses to selection after seven generations. Body length, pronotum width, head capsule width, and fecundity showed consistent, positive correlated responses. Development time showed a negative correlated response. Age at first reproduction showed no consistent correlated response to selection on wing length. These pleiotropic effects among wing length and fecundity, development time, and body size characters provide the potential for these traits to evolve together in O. fasciatus, independently of age at first reproduction.

The effect of host plant phenology on reproduction of the milkweed bug, Oncopeltus fasciatus, in tropical Florida.

A field study of the relationship between host plant phenology and the reproductive pattern of the large milkweed bug, Oncopeltus fasciatus, was conducted in south Florida. Since O. fasciatus need seeds of either milkweed or Nerium oleander plants to reproduce, reproduction takes place on only those host plants that are producing seed pods.Two of four major host plants, Asclepias incarnata and Sarcostemma clausa fruit seasonally, producing pods in early autumn and early winter, respectively. The third milkweed host, Asclepias curassavica, produces almost no pods midsummer (although it flowers abundantly) and few pods midwinter. Nerium oleander (Apocynaceae) produces some pods all year but is only used by O. fasciatus in the summer when milkweeds are not producing pods. Correspondingly, reproduction of O. fasciatus has been observed year round, but relatively few females reproduce in midwinter, coinciding with decreased pod production and low temperatures. This pattern is consistent with the hypothesis that a photoperiodic cue of short day lengths under conditions of cool temperatures may cause adult females to enter diapause and delay reproduction in the field.A comparison of plant phenologies and rainfall between 1976, a very dry year, and 1978, a year with normal rainfall, showed that extreme dryness disrupted the seasonal fruiting of the milkweeds and consequently the reproduction of O. fasciatus.

Competition: Butterflies eliminate milkweed bugs from a Caribbean Island.

By eliminating the food plant, Asclepias curassavica, monarch butterflies, Danaus plexippus, have virtually eliminated milkweed bugs, Oncopeltus spp., from the island of Barbados. The relatively open terrain of Barbados means the plants have no refuge; the butterflies survive on an alternate milkweed food plant, Calotropis procera, whose thick-walled pods make seeds unavailable to the bugs.