Our direct measurements of fecundity made under seminatural conditions in a large population cage in the field lend no support to the dispersal–fecundity trade-off in the Glanville fritillary: the lifetime egg production was higher, not lower, in the more dispersive females from new populations than in the less dispersive females from old populations. Furthermore, the females that were more mobile in the cage tended to have higher lifetime egg production than the less mobile females. These results, which represent perhaps the most inclusive test so far of the dispersal–fecundity trade-off in butterflies, challenge the notion that wing-dimorphic and wing-monomorphic insects would exhibit similar dispersal-related life-history trade-offs.
Rankin and coworkers have previously reported other insect examples of positive correlation between dispersal (long-duration flight) and reproduction, which they expected to be common in species frequently colonizing ephemeral habitats (Rankin & Burchsted 1992). In the migratory but wing-monomorphic grasshopper Melanoplus sanguinipes long-duration flight to exhaustion accelerated the onset of first reproduction and enhanced reproductive success during the entire lifetime. Min et al. (2004) attributed this result to an increased level of juvenile hormone induced by long flight, which is known to be involved in the control of reproduction in most insects.
If high dispersal rate does not lead to reduced fecundity, what might be the physiological and ecological costs? Considering the energetic cost, one possibility is that the more mobile individuals can increase their food intake sufficiently to compensate for the energetic cost of extra mobility. For instance, in the wing-polymorphic hemipteran Sigara, a strong dispersal–fecundity trade-off is apparent under restricted food availability but not under unlimited food availability (Zera & Denno 1997). In our experiment, butterflies fed on the nectar of naturally occurring flowers in the cage, but unfortunately we could not quantify their food intake. It is, however, doubtful whether the less mobile females would have been any more limited by nectar in the cage than the more mobile females. It should also be noted that our comparison between new- and old-population females relates to the known difference in their dispersal rate in the field (Hanski et al. 2002, 2004) rather than to any difference in their mobility in the cage, though there is such a difference in young females (Fig. 1a). Our interpretation of these results is that they reflect general life-history differences between butterflies in new and old populations rather than differential mobility in the cage. On the other hand, we cannot infer from these results what would be the rate of oviposition in the natural landscape, where some females move long distances while others remain in the natal habitat patch. Quantifying the effects of actual long-distance flight on oviposition remains a challenge for the future.
Intriguingly, the present results on oviposition in new- and old-population females are in apparent conflict with our own previous finding on the same species. Hanski et al. (2004) reported a dissimilar scaling of potential fecundity (essentially the number of oocytes at eclosion) with body size in new- and old-population females, yielding greater potential fecundity of large females originating from old than new populations (fig. 4 in Hanski et al. 2004). In the previous study, we recorded 100 oocytes on average per ovariole (SD = 21, n = 91), with a maximum of 164 oocytes (I. Hanski, unpublished). Given the eight ovarioles, these figures give 800 and 1312 as the expected and maximal potential lifetime egg production, assuming that all oocytes are visible at eclosion. These numbers may be compared with those in Fig. 2(d), showing that the top five females managed to lay 800–900 eggs (maximum 916) during their lifetime. Therefore, a small minority of females may have run out of eggs during their lifetime, but the vast majority did not. Given the previous and present results, it is possible that there is some reduction in the number of oocytes at eclosion in the more dispersive females, though there is no difference in the realized lifetime egg production (because females do not generally have a chance to lay all eggs), or the difference is in the opposite direction (implying a difference in the rate of oviposition, as in Fig. 2b,c).
Instead of the expected negative association between dispersal rate and lifetime fecundity, we found a negative association between dispersal rate and maximal life span. We hypothesize that this relationship may reflect variation in the metabolic performance of individuals. Hanski et al. (2004) found that the [ATP] : [ADP] ratio in the flight muscles of female Glanville fritillary following a controlled period of flight was related to population age and spatial connectivity in the same manner as field-measured dispersal rate. Thus the [ATP] : [ADP] ratio was highest in females from new isolated populations and lowest in females from old isolated populations. Hanski et al. (2004) suggested that variation in the [ATP] : [ADP] ratio reflects variation in cellular capacity to renew ATP during flight, and the result would hence imply that a part of the observed variation in dispersal rate is due to variation in the flight metabolic performance of individuals. Recalling that a wide range of studies on various taxa have reported a negative relationship between metabolic rate and life span (for a review see van Voorhies 2001), the reduced life span of the more dispersive butterflies may represent a cost of high metabolic performance. These results suggest that there is a contrast between ‘fast’ females that are dispersive and mature eggs fast, and ‘slow’ females that avoid paying a large cost of dispersal and are superior in surviving a longer time.
differences between the sexes
Variation in dispersal rate and other life-history traits in relation to population age and connectivity is strikingly different in the two sexes in the Glanville fritillary. In contrast to females, new-population males are not more dispersive than old-population males (Hanski et al. 2002, 2004; the present study), nor does the [ATP] : [ADP] ratio (Hanski et al. 2004) or life span in males (Fig. 3b) relate to population age or connectivity. Why should the results be so different for males and females?
One obvious difference between the two sexes lies in the benefit of dispersal to previously empty habitat patches. Females tend to become mated soon after eclosion, and they usually mate only once in their lifetime (Boggs & Nieminen 2004). We found that females that were more mobile in the cage became mated faster than the less mobile females, most likely because males find the more mobile females faster. In any case, most females immigrating to previously empty patches are already mated, and hence males arriving at such patches would have only limited mating opportunities. Males dispersing to existing populations would have better chances of mating, though once again they would mostly encounter mated females. Males born to small populations might do better by dispersing, as there would be limited mating opportunities in small populations and mating with close relatives would lead to inbreeding depression (Saccheri et al. 1998; Haikola et al. 2001). However, whatever the benefits of dispersal in males, the situation is clearly different in female Glanville fritillary in highly fragmented landscapes, where the opportunity to establish new local populations is a major factor selecting for dispersal (Heino & Hanski 2001).
costs and benefits of dispersal and landscape structure
An often-assumed cost of dispersal is high risk of mortality in the landscape matrix (Clobert, Ims & Rousset 2004). In insects that oviposit repeatedly, time and potential opportunities for oviposition are lost during dispersal, even if the rate of mortality would be the same in the matrix and in the habitat. Assuming correlated random walk as the mode of dispersal, the cost of dispersal may be viewed as a trade-off between emigration and immigration: high immigration rate in the more mobile individuals is necessarily associated with high emigration rate, also from a habitat patch at which an individual has just arrived.
Ovaskainen (2004) modelled mark–release–recapture data for Melitaea diamina, a close relative of the Glanville fritillary. He inferred that females spend roughly half of their lifetime in the matrix in a landscape in which the empirical study had been conducted. In this paper, we compared the time spent in the matrix by individuals corresponding to the dispersive butterflies from new populations and to the less dispersive butterflies from old populations in the cage experiment. We found that the direct cost (time spent in the matrix) that the more dispersive butterflies paid in comparison with the more sedentary ones was 4% on average in a representative landscape for the Glanville fritillary. This is not a large cost, but it is important to note that the cost varies greatly depending on local landscape structure, and hence the fitness of butterflies with a particular dispersal phenotype varies from one part of the landscape to another. Spatial variation in landscape structure is thereby a powerful mechanism to maintain variability in dispersal rate and associated life-history traits in real landscapes (Hanski et al. 2004).
Given the assumptions of the movement model, the cost of dispersal may unexpectedly be negative in some parts of a heterogeneous landscape. In our example, the cost was negative in small patches with an intermediate connectivity to other patches. In such situations, butterflies with low r do poorly, because all butterflies regardless of their r are likely to leave a small patch soon, and individuals with low r end up spending much time in the matrix because the natal patch was relatively isolated. Note, however, that if the natal patch is very isolated, the cost is again positive, as now all individuals regardless of their r will be able to reproduce only in the natal patch before dispersal, and individuals with low r would spend more time on average in the natal patch before dispersal.
High or relatively high dispersal rate is expected in species that occur in highly fragmented landscapes consisting of small habitat patches with ephemeral local populations. The Glanville fritillary in the Åland Islands is a prime example (Hanski 1999). None the less, at the individual level high dispersal rate imposes a cost in terms of high emigration rate from suitable habitat, which is reflected in the high frequency of less dispersive phenotypes in old isolated populations (Hanski et al. 2002, 2004). Secondly, the shorter maximal life span of more dispersive females might also select, indirectly, against dispersal especially in more continuous habitats. Weather conditions are commonly unfavourable for mating and oviposition during the adult flight season, making it possibly important to stay alive for a long time. There may be yet other costs and benefits of dispersal that will be detected in closer examination, but the present results conclusively refute the classic dispersal–fecundity trade-off for the Glanville fritillary. We suggest that this trade-off should not be assumed as the default in studies of dispersal and evolution of dispersal in nonmigratory wing-monomorphic insects.