Supplemental Table 1: Raw data: Egg heights and clutch sizes of E. editha in Rabbit
patch-pair
Egg Heights at Rabbit clearing on Collinsia in 1991 (cm). 2.4; 1.8; 1.1; 0.9; 0.9;
0.7; 0.6; 0.5; 0.4; 0.3; 0.3; 0.3; 0.2; 0; 0; 0; 0; 0.(Previously unpublished)
Egg Heights in Rabbit open-forest on Pedicularis in 1993 and 2002: 3.0; 1.1; 0.8;
0.8; 0.8; 0.7; 0.6; 0.5; 0.4; 0.4; 0.3; 0.3; 0.2; 0.2; 0.2; 0.1; 0; 0; 0. (more data in Singer
and McBride 2010)
Clutch sizes at Rabbit in field, estimated to nearest ten when hard to count eggs
wthout breaking up the clutch. Potentially reduced by predation from starting clutch
size.
Clutch sizes in clearing on Collinsia in 1982: 140; 130; 120; 110; 110; 110; 103; 90;
85; 75; 75; 70; 62; 60; 60; 60; 55; 54; 53; 50; 50; 48; 47; 46; 45; 45; 45; 44; 40; 39;
36; 35; 34; 34; 33; 33; 30; 22; 22; 21; 18; 17; 15; 15; 14; 14; 11; 8; 7; 7
Clutch sizes in open-forest on Pedicularis in 1982: 120; 120; 112; 100; 95; 95; 86; 85;
85; 85; 80; 75; 74; 68; 65; 60; 60; 60; 60; 57; 55; 55; 54; 53; 52; 52; 52; 50; 50; 50;
47; 47; 45; 45; 41; 41; 40; 40; 40; 40; 38; 37; 35; 35; 35; 35; 35; 33; 33; 32; 31; 30;
29; 27; 25; 25; 21; 21; 20; 20; 20; 20; 20; 19; 19; 18; 16; 14; 13; 13; 12; 12; 11; 11;
11; 8; 5; 3; 3.
Supplemental Table 2: Qualititative description of host use, host adaptation and hostspecific survival of E. editha in adjacent habitat patches at Rabbit Meadow, 1979-84.
For completeness, table lists minor hosts censused by Singer (1983) but not discussed
in this paper. Details in Singer (1983) Moore (1989), Singer and Thomas (1996),
Thomas et al. (1996), Boughton (1999).
Patch type
open-forest
Hosts
present, in
order of
abundance
Collinsia
Pedicularis
(Castilleja)
clearing
Collinsia
(Castilleja)
(Mimulus)
Butterfly
diet
Butterfly
adaptation
Offspring
survival
98%
Pedicularis
1%
Collinsia
Pedicularis.
strength of
preference
variable; some
individuals
with no
preference
Moderate on
Pedicularis;
Near zero on
Collinsia,
judged from
manipulated
oviposition
Pedicularis;
but evolving:
post-alighting
acceptance of
Collinsia
increased
1984-89
High on
Collinsia,
(1%
Castilleja)
93%
Collinsia
(5%
Castilleja)
(2%
Mimulus)
(moderate on
Castilleja, low
on Mimulus)
Selection
Favors
preference
for
Pedicularis
Collinsia
Appendix 1: Butterfly amenability to studies of dispersal and local adaptation.
The size, manipulability and discrete population structure of many butterflies render
them amenable to studies of dispersal (Ford and Ford 1930; Ehrlich 1961, Hanski
2011). For example, a small team of researchers took less than a month to perform
mark-release-recapture of Euphydryas aurinia across 1,500km2 in the Czech
Republic, incorporating all known populations in the country. They wrote individual
numbers on the wings of 9,118 individuals, recaptured 2,911 and recorded
movements within and among populations (Zimmerman et al. 2011).
Unlike fruit flies, butterflies can be followed as they search for resources.
Their patterns of flight, alighting and resource discovery can be observed and
recorded, revealing the identities of individual plants accepted and rejected for
oviposition. With current technology it is feasible to attach radio transponders to
individuals and track them with harmonic radar (Cant et al. 2005).
That butterflies indulge in local adaptation has become well-known with
respect to mimicry (Jiggins et al. 2001) and, if the Peppered Moth is momentarily
nominated as an honorary butterfly, camouflage (refs in Cook and Saccheri 2013).
Therefore, we also expect to find local adaptation to physical characteristics and
spatial distributions of habitats and the hosts that they contain. These expectations are
fulfilled. Butterflies in one population of M.cinxia clung to an isolated, windy island
by “improving their grip,” evolving stronger claws compared to conspecifics from a
connected landscape (Duplouy and Hanski 2013). In response to a similar problem, a
population of Lycaeides on a windy mountain evolved glue-free eggs that fell off the
host and remained in the habitat when the hosts were blown off the mountain in
winter (Fordyce and Nice 2003).
Local adaptation to selection on butterfly dispersal generates complex suites
of behavioral, genetic and metabolic traits (Hanski 2011; Marden et al. 2013) whose
correlations with known population history are well-replicated in a metapopulation
context (Hanski 2011). Dispersal evolution has been informatively dynamic at range
margins expanding under warming climate (Thomas et al. 2001, Buckley and Bridle
2014) and in anthropogenic landscapes (Ockinger and van Dyck 2012; Stevens et al.
2012). In parallel to these responses to selection on dispersal, local adaptation of
butterflies to their hosts also involves complex suites of rapidly-evolving life-history
and behavioral traits (Singer et al. 1993, Singer and McBride 2010; Bennett et al.
2014).
Cant ET, Smith AD, Reynolds DR, Osborne JL (2005) Tracking butterfly flight paths
across the landscape with harmonic radar. Proc Roy Soc B 272:785-790
De Meeus T, Hochberg ME, Renaud F (1995) Maintenance of two genetic entities by
habitat selection. Evol Ecol 9:131-138.
Duplouy A, Hanski I (2013) Butterfly survival on an isolated island by improved grip.
Biol Lett 9:20130020
Ford HD, Ford, EB (1930) Fluctuation in numbers and its effect on variation in
Melitaea aurinia (Rottembourg, 1775) (Lepidoptera: Nymphalidae). Trans Roy
Ent Soc Lond 78:345-351.
Fordyce, JA, Nice CC (2003) Variation in butterfly egg adhesion: adaptation tolocal
host plant senescence characteristics? Ecol Lett 6:23-27
Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preferenceperformance relationships in phytophagous insects. Ecology Letters 13:383-39
Zimmerman K, Fric Z, Jiskra P et al (2011) Mark-recapture on large spatial scale
reveals long distance dispersal in the Marsh Fritillary, Euphydryas aurinia.
Ecol. Entomol. 36:499-510.
Appendix 2: Discrimination within and among host species, and effects of host
quality and density on butterfly diet.
Example 1: Strong effects of host species on fitness of E. editha were found
when fates of naturally-laid eggs were followed (Moore 1989) and when eggs were
experimentally placed on different plants in the field (Singer et al 1994). Similar
effects appeared in experiments in which growth and survival rates of captive larvae
differed between host species by more than an order of magnitude (Rausher 1982,
Singer and McBride 2010).
We classified as “potential hosts” those species that served as principal hosts
of E. editha at some sites. We then asked how many of these potential hosts were
available to each population and how many were actually used (Singer and Wee
2005). We censused 57 populations across an area of 250 x 1200km and found that
37 of the sites contained more than one potential host, but 43 of the 57 populations
were monophagous. The insects typically failed to use the full range of hosts
available to them: the majority of populations contained abundant hosts that were
used elsewhere but not used at the focal site because they were not locally preferred
(Singer and Wee 2005). These preference differences were important mechanistic
causes of inter-site variation in diet: the butterflies had evolved post-alighting
chemical preferences for different host genera at different sites and any one of five
genera could be the most preferred (Singer 1971, Singer and Parmesan 1993, Singer
et al. 1994; Singer and McBride 2012).
In the same survey of 57 populations the most abundant potential host was
preferred at 19 sites and the least abundant at 12. At the other sites there was either a
tie or no choice. The trend for the most abundant host to be preferred was suggestive
but fell short of significance (p=0.07 by binomial test with expected 50:50
probability) (Singer and Wee 2005).
In 10 of the 57 populations we asked butterflies to rank the actual and
potential hosts in their habitat in order of preference. We then ranked the same plants
in order of their suitability for offspring by manipulating butterflies to lay eggs on
them in the field and recording offspring survival. Of the ten populations, two were
in the throes of rapid diet evolution at the time of the study (Singer et al. 1993). At
these two sites a recently-acquired host was the most suitable but least preferred; in
the other 8 cases the rank order of adult preference was exactly concordant with the
rank order of offspring performance (Singer et al 1994). Since each site contained 3
or 4 hosts, this result represents a highly significant trend for concordance between
preference and performance within the set of 8 “stable” populations. This result
suggests that the quality of hosts had more influence on evolution of preference than
their abundance. The same conclusion was drawn from a recent, separate study in the
Western Sierra Nevada (California) in which E. editha used Pedicularis at some sites
and Collinsia at others in a geographic mosaic, despite the presence of both hosts at
all sites. Plant censuses across this set of sites showed no trend for variation of insect
diet to be associated with variation of host abundance; instead it was clearly
associated with host quality (Singer and McBride 2012).
Example 2: The Glanville Fritillary, M. cinxia, used just two hosts in the Åland
islands: Veronica spicata and Plantago lanceolata. Some habitat patches contained
only Plantago, many patches contained both hosts and a few contained only
Veronica. In most patches where both hosts occurred, both were used by ovipositing
butterflies. Surveys of survival from naturally-laid egg clutches were conducted in
each of 7 years across 1,923 populations (van Nouhuys et al 2003). Mean survival
per clutch was 20 on Plantago and 19 on Veronica, but even this small difference
disappeared when analysis controlled for differences among habitats that might not
necessarily be host-associated. Laboratory experiments showed very large differences
in the ability to support larvae among individual plants within host populations, but no
overall difference between plant species (van Nouhuys et al. 2003).
In sum, despite a great deal of research effort over many years, no evidence
was found of any overall effect of host genus on fitness of M. cinxia: when plants
were categorized taxonomically there was no detectable selection on host use.
However, there WAS substantial heritable variation of post-alighting oviposition
preference for Plantago versus Veronica, which emerged clearly when M cinxia from
different parts of Åland were raised in Texas on a common host and preference-tested
on the same plants (Kuussaari et al. 2000). This difference persisted in the laboratory
for several generations (Singer and Lee 2000); however, differences in maternal
preference were not associated with variation in offspring performance; there was no
preference-performance correlation (van Nouhuys et al. 2003).
If these preference differences arose in the context of the equality of fitness on
the two hosts that was observed, then, by elimination, we expect them to be responses
to host density rather than host quality, resulting simply from the fact that preference
for the more abudant host saves time by shortening oviposition searches. This
expectation was fulfilled: tested post-alighting preferences varied across the
metapopulation in parallel with variation in the relative abundance of the two hsosts
(Kuussaari et al. 2000).
Discrimination within host species: as motivation increases during a search, the
fraction of plants that would be accepted (if encountered) increases within each host
species. For some butterflies, all members of the most-preferred host population are
preferred over all members of the second-ranked species, but frequently there is
overlap of acceptability between host species and insects may respond more strongly
to chemical traits that vary within host populations rather than between different host
species (Singer and Lee 2000). Regardless of this complication, butterflies must
suffer costs when they fail to encounter their most-preferred hosts and are forced to
continue to search until they accept lower-ranked hosts
The E. editha population at Rabbit Meadow contained some individuals that were
specialists with respect to chemical variation within the host Pedicularis population
and others that were generalists. Further, there was a preference/performance
correlation in the strict sense of the term: specialists produced offspring that survived
better on plants accepted by specialists than on rejected plants, while offspring of
generalists survived equally well on plants accepted and ejected by specialists. The
difference between the two classes of offspring in relative performance on the two
plant classes was significant (Ng 1988).