Global Change Biology (2010) 16, 2923–2929, doi: 10.1111/j.1365-2486.2010.02177.x

Adaptation to host plants may prevent rapid responses to climate change

SHANNON L. PELINI1 , JESSICA A. KEPPEL2 , ANN E. KELLEY3 and JESSICA. J. HELLMANN Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA

Abstract We must consider the role of multitrophic interactions when examining species’ responses to climate change. Many plant species, particularly trees, are limited in their ability to shift their geographic ranges quickly under climate change. Consequently, for herbivorous , geographic mosaics of host plant specialization could prohibit range shifts and adaptation when insects become separated from suitable host plants. In this study, we examined larval growth and survival of an specialist butterfly (Erynnis propertius) on different (Quercus spp.) that occur across its range to determine if individuals can switch host plants if they move into new areas under climate change. Individuals from Oregon and northern California, USA that feed on Q. garryana and Q. kelloggii in the field experienced increased mortality on Q. agrifolia, a southern species with low nutrient content. In contrast, populations from southern California that normally feed on Q. agrifolia performed well on Q. agrifolia and Q. garryana and poorly on the northern, high elevation Q. kelloggii. Therefore, colonization of southern E. propertius in higher elevations and some northern locales may be prohibited under climate change but latitudinal shifts to Q. garryana may be possible. Where shifts are precluded due to maladaptation to hosts, populations may not accrue warm-adapted genotypes. Our study suggests that, when interacting species experience asynchronous range shifts, historical local adaptation may preclude populations from colonizing new locales under climate change. Keywords: climate change, geographic mosaic, local adaptation, plant-insect interactions, range shifts, resource specialization

Received 27 September 2009 and accepted 13 December 2009

Insects have been particularly responsive to climate Introduction change because much of their life history is influenced Species have shifted their geographic distributions in by temperature, but they also are strongly affected by response to past and recent climate changes, and these the quality and availability of plants as food resources shifts are expected to continue with future climate (Pelini et al., 2009b). Because insects and plants disperse change (Parmesan & Yohe, 2003). These distributional at different rates, their geographic range shifts during shifts occur as habitats at poleward latitudes or higher periods of climate change could differ substantially elevations become suitable and individuals disperse to (Schweiger et al., 2008). For example, a number of and establish in new locales. The increased frequency of butterfly species have recently shifted their distribu- dispersal from equatorial populations and/or strong tions poleward or to higher elevations (e.g., 240 km over selection against poleward genotypes under a changing 30 years) (Parmesan et al., 1999) while the expected climate has resulted in increases in equatorial geno- average rate that trees can track a changing climate is types toward the poles and could increase the climatic only 20–40 km per 100 years (Davis & Shaw, 2001). This tolerance of poleward populations (Rodrı´guez-Trelles & host plant lag could limit the establishment of insect Rodrı´guez, 1998; Umina et al., 2005; Balanya´ et al., 2006). populations in new regions. Interactions between insects and host plants often vary Correspondence: Jessica. J. Hellmann, tel. 1 1 574 631 0296, fax throughout species’ ranges, and it is important that we 1 1 574 631 7413, e-mail: [email protected] think about this in the context of range shifts under climate change. Geographic turnover in host plant suitability and 1Present address: S. L. Pelini, Harvard Forest, Harvard University, Petersham, MA 01366, USA. availability often results in populations of herbivorous insects that are locally adapted to different host plants 2 Present address: J. A. Keppel, Department of Biology, University throughout the insect’s geographic range, creating a geo- of North Carolina, Chapel Hill, NC 27599, USA. graphic mosaic of host plant specialization (Thompson, 3Present address: A. E. Kelley, School of Natural Resources and 2005). Strong adaptation to local host plants can lead to Environment, University of Michigan, Ann Arbor, MI 48109, USA. reduced fitness on alternate host plants (Boecklen & r 2010 Blackwell Publishing Ltd 2923 2924 S. L. PELINI et al.

Mopper, 1998). Rapid adaptive evolution of novel host (red vs. white oak groups) (Pavlik et al., 2002). Popula- plant use could relax this barrier, but this process may be tions of E. propertius in southern and central California constrained by the rapid pace of modern climate change are multivoltine and feed on the leaves of Quercus (see Etterson & Shaw, 2001; Hellmann & Pineda-Krch, agrifolia (coast live oak) (Fig. 1), an evergreen red oak. 2007). Therefore, equatorial genotypes could be reduced E. propertius populations at higher elevations (600– in frequency or lost if equatorial individuals disperse 1800 m) between southern California and southwestern poleward but fail to colonize because they encounter Oregon feed on Quercus kelloggii (California black oak) unsuitable or less suitable host plants. This could compro- (Fig. 1), a deciduous red oak. Populations north of south- mise poleward or upland populations by limiting the western Oregon are univoltine and feed exclusively on arrival of genotypes adapted to warmer conditions. the only available oak species, (Oregon In this study, we examined the geographic structure white oak or Garry oak) (Fig. 1), a deciduous white oak. of host plant specialization within the geographic dis- Other Quercus species also may be used by E. propertius tribution of Erynnis propertius, the Propertius duskyw- in California, but Q. agrifolia and Q. kelloggii are the only ing (: Hesperiidae) (Guppy & recorded hosts and the most common in sites where Shepard, 2001). E. propertius occurs along the western E. propertius has been collected (personal observations). coast of North America from Baja California, Mexico to Lab experiments revealed that E. propertius has complete British Columbia, Canada where oaks (Quercus) occur mortality on alternate Quercus species, including the (Scott, 1986; Opler, 1999) (Fig. 1). widespread Quercus chysolepis (canyon live oak), how- The three primary Quercus host plant species used by ever (S. L. Pelini, unpublished results). E. propertius offer interesting contrasts in geography The orientation of the transitions in dominance of these (northern vs. southern and low vs. high elevation), host plant species across latitude and elevation is impor- phenology (evergreen vs. deciduous) and phylogeny tant when assessing the capacity for range shifts in E. propertius under climate change, particularly because these Quercus species overlap at their range boundaries. Q. kelloggii co-occurs with Q. garryana at its northern range edge and co-occurs and hybridizes with Q. agrifolia in southern California (Pavlik et al., 2002) (Fig. 1). There areafewplaceswhereQ. garryana and Q. agrifolia overlap in Q. garryana-dominated woodlands (Pavlik et al., 2002), butwedidnotsampleE. propertius from those locations due to small population sizes. In this study, we conducted a fully crossed feeding experiment to determine if E. propertius populations are adapted to local host plants. We assume that the rate of current climate change constrains rapid adaptive evolu- tion of host plant use in E. propertius and that the Quercus host plants will disperse slower than E. propertius.His- torical adaptation to local Quercus host plants could prevent range expansion if southern E. propertius popula- tions have reduced fitness on northern or high elevation host plants. Given an unchanging host plant landscape, host plant limitations could occur for E. propertius in two geographic areas. First, individuals dispersing from south (i.e., those that occur with and use Q. agrifolia) (Fig. 1) to north will have to switch to Q. garryana. Second, individuals dispersing to higher elevations and other northern locales will have to switch to Q. kelloggii.

Materials and methods

Fig. 1 Distribution map of Quercus host plants with Erynnis Feeding trials propertius sampling sites. Quercus distributions are from Little (1971). Triangles represent ‘northern’ sites and squares represent We collected E. propertius individuals from four sites ‘southern’ sites. dominated by Q. agrifolia in southern and central California

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(Qa1–Qa4) (Fig. 1) and from two sites dominated by ous insects that specialize on Quercus are insensitive to, or even Q. garryana in northern California and southwestern Oregon benefit from, tannins (Roslin & Salminen, 2008). (Qg1 and Qg2) (Fig. 1). We also collected individuals from one Leaves were collected from greenhouse Q. agrifolia, Q. kelloggii-dominated locale with Q. garryana in the Sierra Q. kelloggii and Q. garryana plants used in the E. propertius Nevada Mountains of central California (Qk1) (Fig. 1). Eggs feeding trials during July of 2007 and 2008. The leaves were were collected from Qk1, Qg1 and Qg2 (‘northern’) in April– immediately weighed and oven-dried (60 1C for 24 h) and May 2007 and again in April–May 2008. Eggs were collected moisture content was assessed using standard gravimetric from Qa1 to Qa4 (‘southern’) in March–May of 2008. Gravid techniques. Dried leaves were then ground to a fine powder female E. propertius were caught during the first flight of the on a Wiley Mill (40 mesh). Total leaf nitrogen (N) and carbon season with nets and placed in enclosures with Quercus clip- (C) were determined by microcombustion (Costech Analytical pings (Q. agrifolia for southern females and Q. garryana for Technologies, Valencia, CA, USA) and percent lignin was northern females). To maximize egg production in the smallest assessed through acid detergent digestion (Ankom Technol- amount of space, adult females were combined in oviposition ogy, Macedon, NY, USA). cages that were separated by site. Eggs were collected daily To determine if trees grown in the greenhouse had similar and kept in coolers (7–9 1C) during transit to greenhouse properties to field trees, we collected leaves from each of the facilities on the University of Notre Dame campus. Upon three species from multiple individuals at E. propertius sam- arrival, eggs were placed in the greenhouse in common con- pling locations and nearby areas (10–20 leaves/tree, three to ditions. Second instar E. propertius larvae were placed indivi- five trees/site, four sites). Mature leaves of Q. garryana and dually into sterilized 12 cm  8cm 2 cm polypropylene Q. kelloggii were collected in July 2008, and Q. agrifolia leaves of enclosures covered with Dacron chiffon mesh (4 cells mmÀ1) varying ages were collected in March of 2008 to control for and fed sprigs of leaves from one of the three Quercus species. phenological differences between collection dates of decid- Leaves were held in florist aquapics and replaced as needed to uous vs. evergreen species. Upon collection, leaves were ensure an abundant food supply. placed in coolers and shipped to the University of Notre Dame Leaves fed to E. propertius during the experiment were from for chemical assays. Owing to changes associated with ship- potted, nursery stock of Q. agrifolia, Q. garryana and Q. kelloggii ping, moisture content was not assessed for field-collected leaf that were two to five years old. Plants of each species origi- samples. nated from at least two different nurseries that used different collection sites. All greenhouse plants were grown in common soils and conditions in greenhouse facilities at the University Data analysis of Notre Dame. Greenhouse light and temperature controls were set to initiate leaf flush in mid-late March to match Survival and growth of E. propertius and leaf chemistry for typical leaf flush of Q. agrifolia in southern California. This Quercus in the greenhouse did not differ in 2007 and 2008 and date was slightly earlier than leaf flush of Q. garryana and therefore were combined in analyses. Erynnis propertius indi- Q. kelloggii in southwestern Oregon (mid-April). viduals were placed into two larval origin groups for analyses: Upon pupation (June–August) each E. propertius individual southern (Qa1–Qa4) and northern (Qk1, Qg1, Qg2). was weighed and the date of pupation was recorded. We Logistic regression was used to determine if E. propertius measured fitness as survival, pupal mass and time to pupa- populations had reduced odds of surviving on non-natal vs. tion. Faster development times are beneficial for insects be- natal Quercus hosts. We conducted a two-factor multivariate cause they reduce the time that larvae are vulnerable to disease analysis of variance (MANOVA) in Systat 12 (Systat Inc., and predation (Benrey & Denno, 1997), and pupal size is Chicago, IL, USA) to determine if larval origin (southern or strongly correlated with fecundity in Lepidoptera (Boggs, northern), experimental host species (Q. agrifolia, Q. garryana 1986). or Q. kelloggii) or an interaction between the two factors explained variance in pupal mass and ln (time to pupation). We also included collection site (Qa1–4, Qk1, Qg1, Qg2) nested within larval origin group to test for population level differ- ences. Univariate ANOVA and Tukey’s post hoc tests were used Leaf chemistry to test for differences among treatments when appropriate. We Previous experiments with E. propertius revealed that survivor- also performed separate MANOVA on greenhouse and field- ship and growth do not differ on potted vs. wild Q. garryana collected leaves to determine if the Quercus species differed in plants (S. L. Pelini, unpublished results), so we assumed that carbon to nitrogen ratios, and lignin content and moisture host plant effects on E. propertius performance observed in this content. experiment reflected patterns from wild trees. We examined differences in leaf moisture and carbon to nitrogen ratios of leaves of the three oaks grown in the greenhouse because Results moisture and N (or N : C) are positively associated with development rates and survival in insects (Scriber & Slansky, Feeding trials 1981). We also examined differences in lignin, a factor that decreases the palatability and digestibility of leaves (Feeny, Larval origin did have a significant effect on pupal mass 1970). We did not perform phenolic assays because herbivor- (but not time to pupation), with northern individuals r 2010 Blackwell Publishing Ltd, Global Change Biology, 16, 2923–2929 2926 S. L. PELINI et al. being larger than southern individuals across host plant Leaf chemistry treatments (Wilks’l 5 0.86, P 5 0.002). Quercus spe- 2, 87 Leaves of the three Quercus species differed in lignin cies did not have a statistically significant effect on content and carbon to nitrogen ratios (greenhouse: pupal mass or time to pupation (Wilks’ l 5 0.923, 4, 174 Wilks’ l 5 0.36, Po0.001; field: Wilks’ l 5 0.29, P 5 0.136). 6, 54 4, 108 Po0.001) (Fig. 4). Q. agrifolia had reduced leaf moisture Survival on natal vs. nonnatal Quercus host plants relative to Q. kelloggii (F 5 4.38, P 5 0.022) and higher differed for southern and northern individuals. South- 2, 29 carbon to nitrogen ratios (greenhouse: F 5 6.99, ern individuals were less likely to survive on Q. kelloggii 2, 29 P 5 0.003; field: F 5 17.9, Po0.001) and lignin con- leaves than on Q. agrifolia leaves (w2 5 10.36, P 5 0.006) 2, 55 tent (greenhouse: F 5 57.8, Po0.001; field: F 5 (Fig. 2). Northern individuals had reduced odds of 2, 29 2, 55 43.5, Po0.001) than the two deciduous Quercus species. surviving on Q. agrifolia than they did on Q. garryana The two deciduous species, Q. garryana and Q. kelloggii, (w2 5 41.4, Po0.001) (Fig. 2). differed only in lignin content, with Q. garryana having The interaction between Quercus species and larval a higher proportion of lignin in its leaves. origin was statistically significant for pupal mass and time to pupation (Wilks’ l4, 174 5 0.79, Po0.001). South- ern individuals reared on Q. agrifolia were 23% larger, Discussion and conclusion and those on Q. garryana were 24% larger, than those that consumed Q. kelloggii leaves (F2, 88 5 6.14, Our results show that southern E. propertius individuals P 5 0.003) (Fig. 3a). Furthermore, southern individuals that use Q. agrifolia in the field can successfully feed on that consumed Q. kelloggii took 25% longer to reach the northernmost host plant, Q. garryana. However, pupation (F2, 88 5 8.08, P 5 0.001) (Fig. 3b) than those fitness is reduced when southern E. propertius indivi- that consumed Q. garryana. Southern individuals fed duals feed on another northern and high-elevation Q. kelloggii were 32% smaller (Fig. 3a) and took 44% plant, Q. kelloggii, potentially due to a trade-off of local longer (Fig. 3b) to reach pupation than northern adaptation to Q. agrifolia. Therefore, movement of individuals reared on Q. kelloggii. southern E. propertius individuals into upland or north- There were differences in survival and pupal mass ward populations that use Q. garryana likely will not be across southern E. propertius populations. Individuals restricted by host specialization, but movement into from the northern-most southern site (Qa4) had high populations that use Q. kelloggii may be restricted. mortality across treatments (only 4% survival compared However, successful colonization of and adaptation to with 60% by the other southern individuals). Southern Q. kelloggii might occur if southern E. propertius popula- individuals were smaller than northern individuals tion growth rates do not fall below zero despite the (F1, 88 5 13.9, Po0.001), but this was driven by pupae current maladaptation to Q. kelloggii. from Qa4, which were significantly smaller (38%, on Previous work using neutral genetic markers re- average) than northern individuals. In addition, pupae vealed that populations of E. propertius are strongly from QA4 were 34% smaller than individuals from the differentiated, particularly in the northern and southern southern-most site, Qa1, and they were marginally reaches of the species’ range, including locations where smaller than southern individuals from the other two E. propertius was collected for this study (Zakharov & southern, Q. agrifolia-dominated sites (F5, 88 5 2.35, Hellmann, 2008). This limited gene flow across P 5 0.047). E. propertius populations could facilitate adaptation to

Fig. 2 Survival results for southern (left) and northern (right) Erynnis propertius individuals on the three Quercus host plants. Bars are odds of surviving to pupation Æ 95% CI on nonnatal Quercus hosts (Q. kelloggii and Q. garryana for southern and Q. kelloggi and Q. agrifolia for northern individuals) relative to natal Quercus host (Q. agrifolia for southern and Q. garryana for northern individuals) (reference line). Instances where the confidence intervals do not overlap the reference line indicate a statistically significant difference (Po0.05) in performance on natal vs. nonnatal Quercus hosts. These cases are indicated with an asterisk.

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Fig. 3 Larval growth results for southern (left) and northern (right) Erynnis propertius individuals on the three Quercus host plants. Bars are mean pupal mass (g) Æ 95% (a) and mean time to pupation (days) Æ 95% (b). Mean time to pupation data were natural log- transformed for statistical analyses but back-transformed data are shown here. Letters denote statistically significant differences (Po0.05).

Fig. 4 Mean proportion lignin, proportion moisture and C : N Æ SE of greenhouse (a) and field-collected (b) Quercus species. Capital letters distinguish statistically significant differences in C : N; lowercase letters for proportion leaf moisture and capital letters with single quotation mark are for proportion lignin. r 2010 Blackwell Publishing Ltd, Global Change Biology, 16, 2923–2929 2928 S. L. PELINI et al. local host plants as well as to climate. Translocation deciduous Quercus spp., Q. garryana and Q. kelloggii.Of experiments with E. propertius revealed that populations the two deciduous Quercus spp., Q. garryana has 50% from California and Oregon performed better than those more lignin and 20% higher C : N ratios than Q. kelloggii. from Vancouver Island when placed in warm condi- Therefore, the relative suitability of the Quercus hosts tions, suggesting that southern populations are adapted for a given E. propertius population will not change if the to warmer conditions (Pelini et al., 2009a). Consequently, changes in leaf chemistry under climate change are on without increased climatic tolerance associated with the the same order of magnitude as those found in other arrival of southern genotypes, E. propertius populations studies. that currently occur in areas with Q. kelloggii may Some of our findings may be better explained by the respond less favorably to climate change. historic, rather than the current, distributions of the While differences in survival and growth of northern three Quercus species. For example, although southern E. propertius reflected differences in chemistry in the E. propertius populations do not currently encounter three Quercus species (Fig. 4), performance of southern Q. garryana in the field, performance was equally as E. propertius did not. Southern E. propertius individuals high on Q. garryana as it was on their natal Q. agrifolia. were only half as likely to survive (Fig. 2) and had Selection for high performance on Q. garryana in south- significantly reduced growth (Fig. 3) on Q. kelloggii ern populations could have occurred if Q. garryana relative to their natal host, Q. agrifolia. This result sug- previously occurred in southern locales. While the gests that southern E. propertius individuals are locally historical southernmost extent of Q garryana is not adapted to Q. agrifolia, despite its reduced nutrient known, isolated Q. garryana groves and individual trees quality relative to the other Quercus species. The reduced do currently occur in southern California. Alternatively, performance on Q. kelloggii also suggests that there is a selection against Q. garryana use in southern locales trade-off in host use, but we are uncertain which trait(s) could be counteracted by gene flow from northern confers adaptation to Q. agrifolia and maladaptation to E. propertius populations. Q. kelloggii in southern E. propertius populations. It is also We assume that the distribution of Quercus species possible that oak properties (e.g., minerals and other will initially remain relatively unchanged on the time trace elements, secondary compounds, etc.) that were scale of potential E. propertius dispersal and population not measured in this experiment affect the performance establishment under climate change. While Quercus of E. propertius and explain these differences. species experienced range shifts in conjunction with While we are not aware of studies that examine the adaptation during past climate change, shifts during effects of increased CO2 and temperature in these parti- current climate change are expected to be slow due to cular Quercus species, studies on other Quercus species limitations on dispersal and recruitment (Kueppers suggest that Quercus suitability declines (e.g., nitrogen et al., 2005; Marsico et al., 2009). Meanwhile, recent content decreases) under climate change, potentially climate-driven range shifts in other Erynnis species leading to decreased fitness of some herbivorous insects have been recorded (Parmesan et al., 1999), suggesting (Dury et al., 1998; Stiling et al., 2003; Hall et al., 2005). For Erynnis can respond quickly to warming if the situation example, compensatory feeding to circumvent the re- is conducive. duction of nitrogen can cause Quercus feeders to ingest We also assume that rapid adaptive evolution of more defensive compounds such as tannins and lignins. alternate Quercus host use in E. propertius populations For southern E. propertius, increased exposure to defen- will be constrained by the rapid pace of climate change. sive compounds may not cause fitness declines on Evidence of adaptive responses to recent warming has Quercus species that they are preadapted to, i.e., been scarce (Gienapp et al., 2008). Studies have demon- Q. agrifolia, but fitness declines on Q. kelloggii could be strated that evolution can be constrained by correlated exacerbated and fitness on Q. garryana could be reduced traits that are antagonistic to the direction of selection if exposure to defensive compounds increases under imposed by rapid environmental change (Etterson & elevated CO2 and temperature. Shaw, 2001; Hellmann & Pineda-Krch, 2007). Our find- Any changes in leaf chemistry of Quercus hosts under ing of local adaptation in E. propertius does indicate that elevated CO2 and temperature likely will be smaller this species has adapted to different Quercus host plants than the current differences across the three Quercus in the past, suggesting that there is potential for adap- species. For example, other studies found 5%–19% tive evolution of host plant use in the future. However, declines in nitrogen content and 2%–8% increases in the time scale needed for this is likely beyond that of lignin across Quercus spp. under elevated CO2 (Dury suitable climate in historic E. propertius locations. et al., 1998; Stiling et al., 2003; Hall et al., 2005). Our Range shifts in E. propertius could also be hindered evergreen Quercus species, Q. agrifolia, has 20%–80% by phenological mismatches between E. propertius more lignin and 70%–80% higher C : N ratios than the and Quercus host plants. For example, if southern

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