Supplement A: Population dynamics and dispersal in melitaeine butterflies
On the assumption that our study species, Euphydruas editha and E. aurinia, do not differ
in spatial variance of selection, Fst values suggest that E. editha has either greater
5
effective population sizes than E. aurinia or greater dispersal tendency. Can we assess
from the literature whether systematic differences exist between these species in
population dynamics and/or in dispersal tendency?
Population dynamics
10
Melitaeines traditionally have been described as relatively sedentary butterflies (Ford &
Ford 1930, Ehrlich 1965, Kuussaari et al. 1996, Hanski 1999). To the extent that
dispersal of different melitaeines has been studied, it has been similar among species.
Five Finnish melitaeines all had similar patterns of dispersal, as inferred from patch
15
occupancy (Wahlberg et al. 2002). Most convincingly, a metapopulation model in which
dispersal was parameterized from detailed study of a common species, Melitaea cinxia,
accurately predicted patch occupancy in an endangered congener, M. diamina, that was
not amenable to direct study of dispersal (Wahlberg et al. 1996). We don’t have
comparable information on E. aurinia and E. editha, but multiple mark-release studies
20
suggest that the two species are about equally dispersive. Two large-scale markrecapture (MRR) studies of E. editha have been done by Harrison (1989) and of E.
aurinia by Zimmerman et al. (2011). These give us at least some idea of the distances
likely to be covered by individual insects. The very ambitious Zimmerman et al. study
covered 1500km2, marked 9118 insects and recaptured 2911, some of them multiple
25
times. Among those recaptures they recorded 51 insects whose summed lifetime
movements exceeded 5 km and 14 that exceeded 10 km, but these were not straight-line
distances and the maximum straight-line distance covered was shorter, 7.6 km. Harrison
(1989) studied an island-mainland metapopulation of E. editha, with patches distributed
across 300 km2, and maximum recordable movements on the order of 20 km. Patch
30
occupancy patterns showed that colonization of small ‘islands’ occurred quite readily at
short distances from the ‘mainland’, but was “truncated” at around 4.5 km. When 1,000
butterflies were released in non-habitat and forced to search for habitat, 101 were
recaptured and the two longest recorded distances traveled were 5.6 and 3.0km.
While
this study of E. editha is not comparable to Zimmerman et al’s (2011) study of E.
35
aurinia, there is no suggestion in these or other data of an important difference between
the two species in dispersal tendency.
Population density is extremely variable. In both study species, population extinction is
frequent (Ehrlich et al. 1980, Harrison et al. 1988, Parmesan 1996, Anthes et al. 2003,
40
Bulman et al. 2007, Zimmerman et al. 2011), yet both can also reach extremely high
population densities for butterflies. Ford & Ford (1930) documented long-term boom
and bust cycles in an isolated population of E. aurinia and Junker & Schmitt (2010),
using MRR, estimated a population size of about 8,000 Lonicera-feeding E. aurinia
across a study site of 3.6 ha, a density of about 2,200 butterflies /ha. Thomas et al.
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(1996) recorded E. editha densities on the order of one adult per square meter in habitat
patches from which the insects were subsequently extirpated by an unseasonable weather
event. Harrison (1989) captured 1,000 adult butterflies in 14 person-hours of work,
likewise indicating very high density.
50
It's likely that, within each species, ecotypes will differ in population stability and it's
possible that one species may have more overall stability than the other. However,
published evidence shows that the species resemble each other in population dynamics.
Both can reach extremely high local densities, but are critically endangered in parts of
their ranges. Both have colonial structure with patchy distribution across landscapes,
55
sometimes as isolated populations, but more often as metapopulations in which patch
extinctions and colonizations are frequent (Harrison et al. 1988, Thomas et al. 1996,
Joyce & Pullin (2003). Within metapopulations, patch occupancy by Succisa-feeding E.
aurinia was related to patch size, host density, and successional stage of the patch
(Wahlberg et al. 2002a,b). In E. editha, patch occupancy of "islands" in a "mainland-
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island" metapopulation was related to patch size and distance from the mainland
(Harrison et al. 1988).
We might expect the reported high densities to lead to intermittent high dispersal in both
species, but this is not the case among Melitaeines. Both M. cinxia and meadow-ecotype
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E. editha (Bay Checkerspots) were less likely to emigrate when densities were high
(Kuussaari et al 1996, Gilbert & Singer 1973), while dispersal of montane E. editha was
density-independent (Boughton 2000). Studies of E. editha indicated that migrants did
not detect suitable habitat from a long distance and were not able to orient toward it
(Harrison 1989, Boughton 2000). However, a high proportion of migrant E. aurinia did
70
succeed in locating habitat (Washlberg et al. 2002a). These observations don't necessarily
imply a difference between the two species. It is possible that both search randomly
across non-habitat, but are efficient at identifying suitable habitat when they find it.
Assessing differences in dispersal between butterfly species is not simple, since evolution
75
of dispersal tendency is dynamic (Stevens et al. 2010a), varying among individuals and
populations, with mean dispersal changing across short distances and over short time
periods (Gilbert & Singer 1973, Hanski 2011). Classically, MRR in butterflies has given
lower estimates of dispersal than genetic techniques. Practitioners of MRR have tended
to trust their data, impressed by their ability to relocate a moderate proportion of marked
80
insects, often several times during their short lives (of the butterflies, not the researchers).
But what happens to the insects that are not recaptured? No MRR study of E. editha or
E. aurinia has recaptured more than 50% of marked insects, leaving plenty of room for
emigration. In the absence of direct information, the difference between dispersal
estimates obtained from MRR and from genetic studies has long been suspected
85
(especially by the geneticists) to stem from failure of MRR to detect the longest
movements because those movements take animals out of the study area. The
geneticists' case is supported by Zimmerman et al. (2011) who performed MRR on the
marsh ecotype of E. aurinia simultaneously in 110 habitat patches spread across
1500km2. This enabled them to compare estimates of long-distance movement obtained
90
from real observations across a large scale with estimates obtained in traditional manner
by extrapolating from the distributions of distances moved in local studies. They
determined that the extrapolation did indeed underestimate long-distance movement,by a
factor of about two. The local scale predicted more long-distance movement by females
than by males, but in fact, at the larger scale there was no difference between the sexes.
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This can be an important matter because movement among patches by males and females
may carry different implications for gene flow (Forister et al. 2004).
Dispersal of E. aurinia
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MRR has been done on both marsh and scrub ecotypes, and molecular work on the marsh
ecotype. The most extensive study is that of Zimmerman et al. (2011), in which
individual movements of the marsh ecotype reached 10 km. Their large scale study
predicted that 1% of females should travel 4 km, with 0.1% reaching 20 km. Working
with an endangered set of populations in Belgium, Schtickzelle et al (2005) found the
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insects to be quite mobile. In the UK, Warren (1994) wrote that observations of natural
colonizations indicate that the species is "more mobile than previously thought," with a
colonization range of "at least 15-20 km, much more than has been described for other
colonial butterflies." Cowley et al. (2001) ranked E. aurinia 13th out of 44 species of
British butterflies in terms of mobility, with 1 being the most mobile.
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Molecular work on the marsh ecotype has given conflicting results. Joyce & Pullin
(2003), working in 17 Succisa-feeding E. aurinia populations across the UK from
southern England to the Outer Isles of Scotland, found Fst values of 0.012 to 0.10 within
population groups, a mean Fst of 0.16 across the entire set of populations and high genetic
115
diversity (He = 0.267) within populations. There was no significant divergence among
populations less than 20 km apart and no evidence of recent bottlenecks in any of the
populations. Their conclusion was that in each area the insect had a metapopulation
structure within which effective population size was high and local reductions in numbers
were offset by migration.
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In contrast to the UK study, Sigaard et al. (2008) did find evidence of bottlenecks and
drift among "critically endangered" Danish populations of the marsh ecotype. They
found an overall mean Fst of 0.16, the same value as Joyce & Pullin, but over a much
smaller area, with the most distant population pair separated by only about 60 km rather
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than the 800 km in Joyce & Pullin's study. Sigaard et al. (2008) also found significant
differentiation (Fst = 0.10) between populations separated by only 5-6 km. They
expressed surprise at the difference between their results and those of Joyce & Pullin,
wondering whether the cause was that they used microsatellites while Joyce and Pullin
(and all the other studies we cite here) used allozymes. However, they cite several
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studies, including one from butterflies (Meglecz et al. 1998), in which allozyme and
microsatellite analyses gave similar Fst values.
The southern Lonicera-feeding ecotype is not at all endangered, perhaps not even in
decline (Junker & Schmitt (2010). Mean dispersal distances were 53 m for males and 39
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m for females, in a study area where movements of 400 m seemed possible and a few
movements of over 300 m were observed. Sample sizes were high: 2,568 insects marked
with 1,150 recaptures of 735 individuals. The distribution of distances moved showed no
sign of bimodality. More than in most MRR studies, we might have some confidence
that dispersal distances in this case were truly low.
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Dispersal of E. editha
Although E. editha has been subjected to MRR on many occasions, there is no large-scale
study comparable study to the work of Zimmerman et al (2011) on E. aurinia. Ehrlich
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(1965) marked Bay Checkerspots that appeared restricted to small patches of barren
serpentine grassland with very low sward height. He observed that the butterflies
typically turned around when reaching vegetation more than 30cm high in the
surrounding matrix of less toxic sandstone, and his recapture data showed very little
movement between patches separated by 200-300 m. Over a four-year period, he
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recaptured 1021 of 1048 butterflies in their patch of origin, so 2.6% of the recaptured
insects were observed to have moved between patches. In the same study area, Brussard
et al. (1974) observed heterogeneity among individuals in the extent to which they moved
around within a single patch of about 150 x 300 m. Among those captured more than 5
times, some had restricted their movements to 5-10% of the available area in their habitat
155
patch while others ranged across all the entire patch of around 2 ha. Individuals moved
least when densities were highest.
Working with a different set of populations in the same meadow ecotype, Harrison et al.
(1988) described an island-mainland metapopulation structure with a large mainland
160
population numbering several thousand adult insects, surrounded by 27 "islands" of
which seven were colonized, with population size estimates from 10 to 344. Using MRR
and patch occupancy data, they observed movements between patches of 0.1 to 0.9km.
They estimated that a 50% probability of colonization of an island 3 km from the
mainland would require 3 years, 6 km would require 24 years and 8 km more than 50
165
years. In the ten years following extirpation of all the island populations by a drought,
nine colonizations, presumably most occurring from mainland to island, were observed to
occur, across a maximum distance of 4.5 km (Harrison 1989).
These studies give some idea of the ability of the Bay Checkerspot to disperse, recognize,
170
and colonize habitat patches. However, the species E. editha encompasses many
ecotypes, at least one of which is more dispersive than the Bay checkerspot. Gilbert &
Singer (1973) found that Bay checkerspots moved an average of about 47 m between
mark and recapture, and turned around when they encountered shrubby vegetation, while
chaparral-dwelling conspecifics from a habitat only 60 km distant moved an average of
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around 230 m and flew over shrubs without hesitation.
In two separate studies E. editha were not able to navigate efficiently across landscapes
towards preferred habitat patches. Harrison (1989) released Bay checkerspots in nonhabitat at different distances from a habitat patch. She found that the insects moved
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much further and faster through non-habitat than across habitat, but that they moved in
random directions with respect to habitat patches that were 50 m or more distant. They
were not able to orient to distant habitats. Likewise, Boughton (1999) found that
montane E. editha located habitat patches simply by entering them and only then
responded to their quality. When approaching patch boundaries the insects entered
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patches without regard to their quality, but after entering the patches they then emigrated
at a higher rate from the less-preferred patch type.
McKechnie et al. (1975) published data on allozyme frequencies in E. editha, covering
several ecotypes, including the two studied by Gilbert & Singer. They found little genetic
190
differentiation among populations, with mean Fst values (calculated by Slatkin 1985) of
0.06 across all loci. They used prior direct observations of restricted movement in MRR
studies to argue that low Fst values were caused by similar selection acting at different
sites and not by higher migration among them than expected from MRR data. Slatkin
(1985) expressed polite, but strong skepticism of this interpretation. His re-analyses
195
showed that, under the assumption that all populations were evolving independently, all
loci studied by McKechnie et al. would indeed have been under selection, but this
selection would not have favored heterozygotes as the authors claimed. Slatkin's
preferred explanation of weak population differentiation seemed to be that because of
current or recent gene flow, populations were not actually evolving separately, that the
200
calculations of selection at work were invalid for this reason, and that migration was the
main factor responsible for the level and nature of between-population genetic
divergence.
205
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