Biol Invasions (2015) 17:1683–1695 DOI 10.1007/s10530-014-0826-7

ORIGINAL PAPER

Modeling the decline and potential recovery of a native butterfly following serial invasions by exotic species

Tegan A. L. Morton • Alexandra Thorn • J. Michael Reed • Roy G. Van Driesche • Richard A. Casagrande • Frances S. Chew

Received: 14 November 2013 / Accepted: 9 December 2014 / Published online: 27 December 2014 Ó Springer International Publishing Switzerland 2014

Abstract Population sizes and range of the native enabled P. oleracea to adapt to A. petiolata.We butterfly oleracea declined after habitat loss and simulated scenarios of trait proliferation via sponta- parasitism by an exotic braconid wasp (Cotesia neous mutation or immigration of the trait, and glomerata) introduced to control the exotic invasive residual variation in the trait following the butterfly’s butterfly . Further declines are attributed isolation in North America. Results indicate that the to the invasive exotic weed garlic mustard (Alliaria most likely scenario for the population that has petiolata), an oviposition sensory trap on which adapted to garlic mustard includes (1) a change in P. oleracea larval survival and growth are very poor. selection following garlic mustard invasion to favor But a population of P. oleracea has adapted to garlic previously neutral residual variation in the population, mustard over the past several decades, coincident with (2) release from parasitism, and (3) evolution of the introduction of a second parasitoid, C. rubecula,a improved larval survival on garlic mustard, which specialist on P. rapae that is competitively dominant allowed an increased host range, and potentially, to C. glomerata. We used stochastic simulation population size. models to assess the plausibility of a hypothesis that reduced parasitoid pressure over this time period Keywords Enemy-free space Á Pieris Á Tri-trophic interaction Á Novel host Á

T. A. L. Morton Á A. Thorn Á J. M. Reed Á F. S. Chew (&) Department of Biology, Tufts University, Medford, MA 02155, USA Introduction e-mail: [email protected]

A. Thorn The spread of exotic species into an ecosystem can Institute for the Study of Earth, Oceans, and Space, shift selection pressures for native species (e.g., Lau University of New Hampshire, Durham, NH 03824, USA 2006). In herbivore-plant associations, these shifts might be predicted from knowledge of the R. G. Van Driesche Department of Entomology, Plant, Soil and Insect phylogenetic constraints of the herbivore-plant sys- Sciences, University of Massachusetts, Amherst, tems involved (Pearse and Altermatt 2013), may incur MA 01002, USA fitness costs for native herbivores (Nakajima et al. 2014), may have effects that span trophic levels R. A. Casagrande Department of Plant Science and Entomology, University (Harvey et al. 2010a, b), and can involve both of Rhode Island, Kingston, RI 02881, USA ecological and evolutionary processes in communities 123 1684 T. A. L. Morton et al.

(Strauss et al. 2006; Forister and Wilson 2013). We competitively dominant to C. glomerata (Laing and hypothesize here that sequential introductions of two Corrigan 1987; Herlihy et al. 2012), greatly lowering exotic species exerting negative top-down and bot- the abundance of C. glomerata from habitats where it tom-up effects on a native herbivorous insect were was abundant previously (Van Driesche 2008; Herlihy responsible for the native’s decline, but a third et al. 2012), and potentially creating enemy-free space introduction released top-down pressure, creating for the native butterfly. This enemy-free space would opportunity for proliferation of an allele that allows allow slow-growing individuals on garlic mustard, successful dietary expansion by the herbivore, with which would otherwise experience increased exposure positive consequences for its population size. to parasitism and almost certainly be parasitized, to The native butterfly Pieris oleracea Harris (Lepi- survive to pupation and contribute their genetic doptera: ) decreased in abundance and range material to future generations. in eastern and central North America in the late 1800s The serial invasions described above, in tandem (Scudder 1889; Longstaff 1912; Klots 1951; Opler and with variation among butterfly maternal families in Krizek 1984) and is now listed as threatened in parts of larval ability to develop on garlic mustard (Keeler and its range (Massachusetts Natural Heritage and Endan- Chew 2008), could potentially permit P. oleracea to gered Species Program 2010). Declines are attributed expand its host range to include garlic mustard by to decreased native host availability caused by habitat permitting persistence and proliferation of adapted loss (Chew 1981), and especially to parasitism by genotypes. Indeed the population in one locality has Cotesia glomerata (L.) (Benson et al. 2003), an exotic already begun to include garlic mustard in its diet and braconid parasitoid introduced in the 1880s as biolog- its population size is apparently recovering (Chew ical control for the exotic pest Pieris rapae (Clausen et al. 2012). We used a stochastic simulation model to 1978). Invasion by garlic mustard (Alliaria petiolata investigate plausibility of our hypothesized scenario in [Bieb.] Cavara & Grande) following habitat loss and enabling the spread of adaptation to garlic mustard. disturbance likely exacerbated the decline (Courant Specifically, we sought to evaluate the likelihood that et al. 1994; Keeler et al. 2006). Garlic mustard is an (1) observed adapted individuals arose from: a spon- exotic invasive plant first documented in North taneous dominant mutation producing heterozygotes America in 1868 (Nuzzo 1993). It is a sensory trap in the population (or a dominant allele introduced via for P. oleracea. Its aliphatic glucosinolates are cues immigration); or residual variation from dissected for egg laying by P. oleracea (Huang et al. 1995; polymorphism (Bowden 1979) in the Holarctic species Chew and Renwick 1995), and are similar to those of a complex P. napi. We examined the likelihood that the native host (=Dentaria) diphylla (Feeny number of such adapted individuals in a population of and Rosenberry 1982). However, P. oleracea larvae mostly wild-type (non-adapted) individuals would did not survive on garlic mustard (Bowden 1971)or increase and persist. Scenarios evaluating the ecolog- survived poorly and grew slowly (Courant et al. 1994; ical context of such proliferation and persistence of Courant 1996). The ability to use garlic mustard adapted individuals included (2) whether top-down behaves as a dominant, autosomal trait in European regulation in the form of the exotic, generalist P. napi L. (Bowden 1971), a related species in the parasitoid C. glomerata could limit proliferation of Holarctic Pieris napi complex (Bowden 1979; Chew an allele introduced through the scenarios above; and and Watt 2006). F1 hybrid larvae of crosses between (3) whether release from parasitism via introduction of the adapted P. napi with North American P. oleracea the competitively dominant, specialist parasitoid develop on garlic mustard (Bowden 1971). C. rubecula could allow for allele proliferation. Further complicating our expectations about poten- tial proliferation of a trait allowing P. oleracea to develop on garlic mustard is another parasitoid wasp, Methods Cotesia rubecula (Marshall), which was introduced in 1988 as another biological control agent for P. rapae Model overview and parameters (Van Driesche and Nunn 2002). This parasitoid does not attack P. oleracea (Brodeur et al. 1996; Van For our analyses we modified the published stochastic Driesche et al. 2003). Interestingly, C. rubecula is population simulation model of Keeler et al. (2006; 123 Modeling the decline and potential recovery of a native butterfly 1685

Fig. 1 A graphical representation of the life cycle of the native community parameters affecting abundance of each life cycle butterfly P. oleracea modified from Keeler et al. (2006), stage are depicted on each side, along with the corresponding including variables that decrease or potentially decrease equation numbers that describe the relationships of the variables survivorship of individuals. Surviving individuals were tracked to determine survivorship among life-history stages. Survivor- by genotype in separate, but identical models, which interacted ship on garlic mustard Alliaria petiolata (shaded) differs among between generations with random mating. Life history and genotypes

Fig. 1). This model simulates females only. All parasitoid, C. rubecula, so we included this in some parameter values are specified below, and, unless scenarios of our model. Thus, the first significant otherwise noted, are the same as those used in the modification to the existing model was to capture the original model (Keeler et al. 2006; see therein for effect of decreased C. glomerata parasitism as references). The model was built and modified using C. rubecula invades (Brodeur et al. 1996). We also STELLA software (version 8, isee systems, Inc., New increased the number of instars that are separately Hampshire, USA). The original model included top- modeled in the second generation (Fig. 1) to allow us down regulation by the exotic braconid parasitoid, to model decreasing risk with increasing larval instar C. glomerata. Although in the original model, Keeler because susceptibility is size-dependent (Brodeur et al. (2006) concluded that parasitism by C. glomerata et al. 1996; Herlihy et al. 2012). Since larvae develop alone could not cause butterfly extinction, they did at a slower pace on garlic mustard than on native show that parasitism could exacerbate the damaging crucifers (Courant 1996; Keeler and Chew 2008), we effects of garlic mustard invasion on P. oleracea also simulated an increased parasitism risk for those (Keeler et al. 2006). The original model did not, larvae on garlic mustard as a function of exposure however, include the potential effects of the second time. 123 1686 T. A. L. Morton et al.

The second major modification we made to the model was to simulate genetic variation for larval adaptation to garlic mustard, as determined by the alleles R (dominant, resistant or adapted allele allow- ing caterpillar development) and r (recessive, wild- type or susceptible allele). Based on hybridization studies with closely related P. napi (Bowden 1971), we assumed an autosomal dominant allele that allowed larvae to complete development on garlic mustard. Within each generation we simulated changes in the number of individuals of each of three genotypes (RR, Rr, and rr). We simulated random mating among surviving genotypes at the end of each generation using allele frequencies calculated accord- Fig. 2 List of model scenarios, 1 through 5b in the right hand ing to Hardy–Weinberg expectations to determine the column, that we evaluated. Circles and squares adjacent to distribution of alleles among genotypes in the follow- scenario numbers show the starting conditions and ecological ing generation. We pursued a model of random mating variables manipulated in each. Shaded circles indicate the method of introduction of the dominant allele via heterozygotes. based on lack of data suggesting assortative mating An absolute number of heterozygotes represents scenarios according to this trait. But we note that assortative simulating spontaneous mutation, whereas percentages indi- mating by a host could occur if host-determined cated scenarios simulation residual polymorphism in the trait. growth rates cause cohorts growing on the novel plant Shaded squares show which variables were manipulated in each scenario. Specifics on values changed in relevant scenarios are to enclose and mate at a different time from the rest of given in the text. An additional scenario was run beginning with the population (Forister and Scholl 2012). Survivor- 3,000 individuals of each genotype (not depicted) ship on garlic mustard was varied among the three genotypes, as described below. probability of proliferation and persistence of the allele, In each model run, population size was recorded at an extra scenario was run beginning with 3,000 the start of each year of simulated time, and our time individuals of each genotype. These scenarios begin- horizon was 50 years. Each scenario was run at each of ning with 3,000 individuals of each genotype are useful 11 levels of garlic mustard ground cover (from 0 to for comparison to document what specific variables 100 % at 10 % intervals). Each combination of contribute to the decline of garlic mustard-adapted conditions and garlic mustard cover was run 1,000 individuals; however these are not depicted in the times. The 1,000 runs were used to generate a scenario schema (Fig. 2). probability of persistence for each genotype; i.e., the To simulate spontaneous mutation of a resistance percentage of the 1,000 runs with an extant population allele, simulations began with one (Scenario 1, Fig. 2) at the end of 50 years. or five heterozygotes (Scenario 2, Fig. 2). Addition- ally, a similar scenario was run in which one hetero- Model scenarios zygote was reintroduced into the population every year to simulate immigration of adapted individuals (Sce- In all scenarios (Fig. 2), survival of larvae with a nario 3, Fig. 2). Stochastic reintroductions of mutants dominant allele on garlic mustard (SGM,RR or Rr) was were simulated at annual probabilities of 1/3,001, equal to the probability of survival on native crucifers 1/1,000 and 1/100 (results not shown). To model a

(SNC). Survival on garlic mustard was equal to zero for residual polymorphism, simulations began with het- homozygous recessive individuals (SGM,rr). erozygotes comprising 1 % (30 individuals; Scenario Variants on five scenario types (Fig. 2) were run 4, Fig. 2) or 5 % (150 individuals; Scenario 5, Fig. 2) with differing initial population sizes of the three of the total population of 3,000 individuals; the genotypes. All scenarios, unless explicitly stated below, remaining individuals were homozygous recessive. began with 3,000 homozygous recessive (wild-type, In scenarios simulating spontaneous mutation (one non-adapted) individuals. To generate a comparison or five heterozygotes, Scenarios 1–2) and residual useful for indicating the upper bounds of the possible polymorphism (1 or 5 % heterozygotes, Scenarios 123 Modeling the decline and potential recovery of a native butterfly 1687

4–5), parasitism in the second generation was added As with the original model (Keeler et al. 2006), we (Scenarios 1a, 2a, 4a, 5a, Fig. 2). Finally, to simulate included density dependence of emigration (their effects of the invasion of the specialist parasitoid Eq. 2), and we used the same process for the C. rubecula, a set of scenarios decreased parasitism distribution of larvae on plants (their Eqs. 4 and 5). over time to zero halfway through the simulated The number of first instar larvae in the first generation

50 years (Scenarios 1b, 2b, 4b, 5b, Fig. 2). (II,1) is the lifetime fecundity of females, times the hatching success of the first generation (H1 = 0.73 ± 0.073): Model structure

II;1 ¼ Ef à H1 ð5Þ Each simulated year begins with the emergence of females in the first generation, and there were two The number of fifth instar larvae produced in the butterfly generations per year (Fig. 1). The number of first generation (IV,1) is modified from Keeler et al. eggs produced each generation was calculated sepa- (2006) to allow survival on garlic mustard: rately for each genotype. The numbers of female heterozygote eggs (ERr), homozygous dominant eggs IV;1 ¼ II;1 À½II;1 à GM Ãð1 À SGMފ (ERR), and homozygous recessive eggs (Err) were À½II;1 Ãð1 À GMÞÃð1 À SNCފ calculated, respectively, as: ÀðII;1 à GM à SGM à XÞ  À½I Ãð1 À GMÞÃS à XŠ Ef à Ni;Rr à FRr à D ÂÃI;1 NC ERr ¼ Àl ÀÁ2 þ ÂÃII;1 à GM à SGM à X ÃððÞ1 À GMÞÃe Àl þ ÀÁEf à Ni;RR à FRR à D à qi þ ÂÃII;1 Ãð1 À GMÞÃSNC à ðÞÃX Ãð1 À GMÞ e þ E à N à F à D à p þ R ð1Þ Àl f i;rr rr i þ ÂÃII;1 à GM à SGM ÃðX à GMÞÃe Àl ÀÁ þ II;1 Ãð1 À GMÞÃSNC ÃðX à GMÞÃe ERR ¼ Ef à Ni;RR à FRR à D à pi  pi ð6Þ þ Ef à Ni;Rr à FRr à D à ð2Þ 2 That is, the number of fifth instar larvae is the number ÀÁ of first instar larvae (II,1), minus the number of larvae Err ¼ Ef à Ni;rr à Frr à D à qi  q on garlic mustard and on host plants that die, minus the þ E à N à F à D à i ð3Þ f i;Rr Rr 2 number of larvae on garlic mustard and on native host plants that leave due to co-occupancy, plus those Here E is the lifetime number of female eggs f larvae that survive on garlic mustard and native host produced per female (determined from empirical data plants, leave due to co-occupancy, and find an empty as 114 ± 42 SD, see Keeler et al. 2006), and we native host plant, plus larvae that survive and leave the assumed an equal primary sex ratio; F is the g initial garlic mustard and native host plants and find an proportion of females of genotype g not emigrating empty garlic mustard plant. Here, GM is the propor- from the population and is calculated as a density- tion of larvae on garlic mustard, and S and S are dependent function as in Keeler et al. (2006); D is the GM NC survival rates on garlic mustard and native plants, proportion of days suitable for oviposition (based on respectively, calculated by genotype. A value of weather; see Keeler et al. 2006 for description); N is i,g S = 0.388 ± 0.167 was used, identical to that in the number of females in generation i of genotype g; R NC the original model. All stochastic variables without is the number of heterozygotes added to the genotype distributional data were modeled based on a normal population due to spontaneous mutation; and p is the i distribution with 10 % standard deviation about the proportion of the population with dominant alleles, mean (as did Keeler et al. 2006). The survival rate on which is calculated as: garlic mustard for adapted genotypes (SGM,RR and

½ð2 à Ni;RRÞþNi;RrŠ SGM,Rr) was equal to that for survival on native pi ¼ ð4Þ crucifers. Survival on garlic mustard of the wild-type ½ð2 à Ni;RRÞþð2 à Ni;RrÞþð2 à Ni;rrފ (SGM,rr) was always equal to zero. X is the probability The proportion of the recessive allele, qi,is of a plant having more than one (calculated qi ¼ 1 À pi. based on a Poisson distribution in the first generation, 123 1688 T. A. L. Morton et al. hi and on a negative binomial distribution in the second 2 III;2 ¼ II;2 à GM à ðÞ1 À CII generation), and l is the mean number of larvae on a Âà plant (see Keeler et al. 2006 for calculations). þ II;2 à ðÞÃ1 À GM ðÞ1 À CII ð8Þ The number of first instar larvae produced in the hi 2 second generation (II,2) is: IIII;2 ¼ III;2 à GM à ðÞ1 À CIII hi Âà þ III;2 à ðÞÃ1 À GM ðÞ1 À CIII ð9Þ I ¼ E à H à GM à ðÞ1 À C 2 I;2 ÂÃf 2 I In scenarios that included the competitive exclusion of þ Ef à H2 à ðÞÃ1 À GM ðÞ1 À CI ð7Þ C. glomerata by C. rubecula over time (t, in years, That is, the number of first instar larvae is a function of starting with year 0), we modeled the decline in the number of eggs in the second generation on garlic caterpillar parasitism rate (C) as a negative mustard, times hatching success (H2 = 0.53 ± exponential: 0.053), times the proportion of larvae on garlic t mustard that escape death due to Cotesia parasitism C ¼ ðÞCI À x ð10Þ

(1-CI), plus the number of eggs in the second where CI is the parasitism rate for instar I, and generation laid on native hosts, times hatching x = 0.05. success, times the proportion of larvae that escape The number of fifth instar larvae in the second death due to parasitism. Larvae develop more slowly generation (IV,2) is: on garlic mustard than on native crucifers (Keeler and

Chew 2008) and in our model we included this longer IV;2 ¼ IIII;2 À½IIII;2 à GM Ãð1 À SGMފ exposure time to parasitism for larvae feeding on À½IIII;2 Ãð1 À GMÞÃð1 À SNCފ garlic mustard. Thus, the proportion of larvae on garlic ÀðI à GM à S à XÞ mustard that escape parasitism is squared to represent III;2 GM À½IIII;2 Ãð1 À GMÞÃSNC à XŠ the smaller fraction that escaped parasitism on garlic "# k mustard. The values for parasitism rate were derived k þ IIII;2 à GM à SGM à X Ãð1 À GMÞà from Brodeur et al. (1996), who reported C. glomerata k þ m "# parasitism rates in European P. napi for early and late k k larval instars and Herlihy (2012) for P. oleracea.We þ IIII;2 Ãð1 À GMÞÃSNC à X Ãð1 À GMÞà k þ m assumed that each instar stage lasted 3 days and "# plotted the data, followed by creating a linear fit to k k þ I à GM à S ÃðX à GMÞà describe the decline in parasitism rate with increasing III;2 GM k þ m "# instar. We then calculated a parasitism rate for each  k k instar by using the line of best fit to calculate the þ I Ãð1 À GMÞÃS ÃðX à GMÞà III;2 NC k þ m predicted parasitism rate at 1.5 and 4.5 days of development for the first and second instars, respec- ð11Þ tively. Although documented in the laboratory for European P. napi (Brodeur et al. 1996), C. glomerata So, fifth instar larvae abundance is a function of the in the field do not appear to parasitize larvae after the number of third instar larvae, minus the number of second instar in the North American native butterfly larvae that die on garlic mustard and on native hosts, (Herlihy 2012, R. Van Driesche, pers. obs.) so the minus those larvae that survive on garlic mustard and parasitism in the third instar (CIII) was set to zero in all native hosts but leave due to plant co-occupancy, plus scenarios. The estimated parasitism rates for first two those larvae that survive on garlic mustard and on instars was calculated as CI = 0.6425, and native crucifers that leave and find an empty native CII = 0.4433, respectively. host, plus the number of larvae that survive on garlic The number of second and third instar larvae in the mustard and native hosts that leave and find an empty second generation (III,2 and IIII,2, respectively) is the garlic mustard plant. The final four bracketed terms of number of previous instar larvae on garlic mustard and Eq. 11 model the negative binomial distribution of on native host plants that escape death due to parasitism: larvae on host plants, where k is a clumping factor; in

123 Modeling the decline and potential recovery of a native butterfly 1689 the absence of data for this species, we used Harcourt’s (1961) estimate for P. rapae, which similarly lays solitary eggs. The number of pupae (Pu) in each generation is the number of fifth instar larvae times the pupation success rate (U = 0.83 ± 0.083):

Pu ¼ IV;i à U ð12Þ The number of emerging females in the second generation (N2) is determined by the number of pupae not entering diapause (O) times emergence success (M = 0.41 ± 0.041): Fig. 3 Probability of persistence of the homozygous dominant (RR) genotype for scenarios simulating spontaneous mutation of N2 ¼ Pu Ãð1 À OÞÃM ð13Þ the resistant allele within a population at variable numbers and frequencies. A simulation beginning with 3,000 mutant indi- If surviving pupae from the first generation do not viduals is used for comparison to the upper-bounds of develop directly to adults, they enter diapause and persistence and establishment that could be expected. These overwinter. All pupae of the second generation scenarios depict the likelihood of resistant individuals becoming overwinter in diapause and emerge the following established in simulations beginning with 1 heterozygote (Rr = 1), 5 heterozygotes (Rr = 5), and when the mutation spring. Thus, the number of emerging females the occurs each year (Rr = 1/year), or a continual reintroduction of following year is the number of pupae from each the mutation. We assumed survival on garlic mustard was equal generation emerging from diapause, times the over- to that on native hosts for individuals with one copy of the dominant allele. Each data point represents the probability of winter survival rate (SW = 0.169 ± 0.0169): ÂÃpersistence, which is defined as the proportion of 1,000 runs N ¼ S ÃðPu à O ÞþðPu à O Þ ð14Þ with an extant population at the end of the 50 years of the 1;tþ1 W 1;t 1;t 2;t 2;t simulation

cover (Fig. 3). Raising the initial number of hetero- Results zygotes to five individuals (Scenario 2) substantially increased resistant population persistence once garlic In all scenarios, once garlic mustard cover reached mustard cover reached 20 %; persistence peaked at approximately 50 %, the wild-type (rr) butterflies intermediate garlic mustard cover values (Fig. 3). disappeared from the population (identical to results Reintroduction of the mutation as one heterozygote reported by Keeler et al. 2006). Consequently, the per year (Scenario 3) increased persistence to levels heterozygous population crashes soon after the homo- virtually indistinguishable from the scenario starting zygous recessive (wild-type), because the proportion with 3,000 resistant, heterozygous individuals, once of heterozygote genotypes declines as the frequency of garlic mustard cover reached 20 % (Fig. 3). Subse- the wild-type r allele declines, and the (dominant) quent scenarios with the stochastic annual introduc- resistant allele approaches fixation in the population. tion of the mutants to the population at an annual Because our interest is in the persistence of the probability of 1/3,001, 1/1,000 or 1/100 (purposefully resistant allele, we show only the results of the unrealistically high mutation rates) did not produce homozygous dominant portion of the population to results different from simulations beginning with one illustrate the important trends. mutant and no subsequent introductions. For all scenarios except those beginning with 3,000 Parasitism substantially decreased the probability heterozygous individuals, there was no proliferation or of persistence for populations starting with one or five persistence of homozygous dominant individuals at mutants (Fig. 4). Parasitism amelioration (creation of 0 % garlic mustard cover. Simulations beginning with enemy-free space) by the introduction of C. rubecula one mutant individual (Scenario 1) had a low (\10 %) had little effect on persistence for simulations begin- probability of persistence for the homozygous dom- ning with a single mutant (Fig. 4). The effect was inant genotype under all scenarios of garlic mustard stronger for simulations beginning with five mutants,

123 1690 T. A. L. Morton et al.

Fig. 4 Probability of persistence of the homozygous dominant resistant individuals becoming established and persisting under (RR) genotype. a Scenarios where parasitism was absent (gray conditions of no parasitism, constant parasitism, and a decline in lines) or present in varying levels of treatment (constant over parasitism over time. c Scenarios examining a residual time, or decreased to zero halfway through the simulation time) polymorphism of 5 % (150 heterozygotes) of the total combined with spontaneous mutation levels. Scenarios depict population of 3,000 individuals. Each data point represents the the likelihood of resistant individuals becoming established probability of persistence, which is defined as the proportion of under conditions of the resistant allele conferring survival on 1,000 runs with an extant population at the end of the 50 years of garlic mustard equal to that on native host plants. Lines represent the simulation. Gray lines represent the upper- and lower bounds simulations beginning with 1 or 5 mutants for each of the of probability of establishment and persistence expected based parasitism treatments. b For scenarios examining a residual on simulations with high (3,000) and low (1) number of polymorphism of 1 % (30 heterozygotes) of the total population heterozygotes at the beginning of the population for comparison. of 3,000 individuals, gray lines represent the upper- and lower- Black lines indicate the probability of resistant individuals bounds of probability of establishment and persistence expected becoming established and persisting under conditions of no based on simulations with high (3,000) and low (1) number of parasitism, constant parasitism, and a decline in parasitism over heterozygotes at the beginning of the population for comparison time (also depicted in Fig. 1). Black lines indicate the probability of

123 Modeling the decline and potential recovery of a native butterfly 1691 with persistence [20 % when garlic mustard cover resistant population. Based on these results, we was 30–70 % (Fig. 4). However, this persistence rate conclude that a larger number of heterozygotes would was not increased by more than approximately 5 % be required for a greater than 50 % likelihood of compared to persistence without amelioration (Fig. 4). persistence at moderate cover of garlic mustard. With Scenarios simulating residual polymorphism (Sce- very high and very low garlic mustard cover, we found narios 4–5) showed the likelihood of resistant indi- that resistant individuals proliferated much more viduals persisting was higher than that exhibited by slowly, perhaps due to encounter rates that either mutation, but lower than that modeled for annual overwhelm the population’s ability to generate resis- immigration. When beginning with 1 % (30 individ- tant individuals or fail to exert sufficient selective uals) of the population heterozygous for the resistant pressure (Forister and Wilson 2013). Larval perfor- allele, homozygous dominant individuals persist at mance on garlic mustard varies widely among mater- levels close to the upper expected bound (i.e., when nal families; laboratory rearing shows that several beginning with 3,000 heterozygous individuals) when resistant offspring could arise in one generation from garlic mustard cover is 20 % or higher (Fig. 4). one mother (Keeler and Chew 2008). Based on our Constant parasitism substantially decreases the prob- simulations, small groups of heterozygous offspring ability of persistence, although a decline in parasitism arising in a single generation could cause establish- over time (due to enemy release) increases the ment and persistence of a garlic mustard-resistant probability of persistence by approximately 10 % at population in the presence of the favorable selective every level of garlic mustard ground cover above 0 % pressure caused by moderate levels of garlic mustard (Fig. 4). We found similar patterns for scenarios cover. beginning with 5 % of the population polymorphic for One alternative we evaluated is whether persistence garlic mustard resistance, although the absolute values of a resistant genotype would be more likely if it were of probability of persistence are consistently higher a residual polymorphism. Simulations beginning with (Fig. 4). a polymorphism of 1 or 5 % of the total population carrying the resistant allele showed substantial prob- abilities of persistence close to those estimated by Discussion simulations beginning with 3,000 heterozygotes. This is a higher likelihood of persistence than occurred in We used simulation modeling to investigate the our mutation scenarios, suggesting that any docu- expansion of diet by a native butterfly P. oleracea mented adaptation is more likely to be the result of via proliferation of an extant but previously selectively selection operating on residual polymorphism than on neutral genotype, in the presence of the serial spontaneous mutation. The possibility of residual invasions of three introduced species. Of these exotic polymorphism is supported by our rearing garlic species, two exert respectively negative bottom-up mustard-adapted larvae from a few mothers collected and negative top-down effects on the native butterfly, in Vermont, where P. oleracea populations have not and the third contributes to amelioration of negative (yet) been exposed to garlic mustard (Keeler and top-down effects, creating enemy-free space for the Chew 2008, Chew, unpublished data). Because inter- butterfly. The predicted effects of a suite of tri-trophic specific pairings with P. rapae have not been observed interactions under various scenarios of resistance in the field (Chew 1981), adaptive variation introduced prevalence show a wide range of possible outcomes, by introgression (Hedrick 2013) from this garlic ranging from extinction to a high likelihood of a mustard-adapted species seems unlikely. persistent population of native butterflies adapted to Top-down pressure on P. oleracea from C. glomer- the exotic, invasive host plant. ata parasitism substantially decreases the probability When we evaluated scenarios in which one mutant of persistence of adapted individuals. For scenarios (a heterozygous resistant individual) arises, we found beginning with five mutants, this probability never that a resistant population failed to establish and exceeded 20 % in our models, even in cases where persist. Increasing the initial number of mutants to five parasitism is reduced significantly and eliminated over individuals is sufficient to cause a substantial increase time to simulate C. rubecula displacement of C. glom- in the probability of persistence of a homozygous erata. In contrast, for scenarios of residual 123 1692 T. A. L. Morton et al. polymorphism, parasitism does not cause complete an exotic, invasive host plant (Keeler et al. 2006). extinction of adapted individuals (i.e., probability of Similar evolutionary traps (sensu Schlaepfer et al. persistence[0 %); however the probability of persis- 2002) have been documented for other , tence is substantially reduced, especially at high levels including the silkmoth Hemileuca sp. and the wetland of garlic mustard cover. Contrary to expectations, plant Lythrum salicaria (Gratton 2006), and the eliminating parasitism over time did not increase monarch butterfly Danaus plexippus and swallow- persistence likelihood to the result from no-parasitism worts Vincetoxicum nigrum (Casagrande and Dacey levels, although the likelihood of persistence of the 2007). Our results show a possible escape route from homozygous resistant genotype increased approxi- this type of evolutionary trap: release of top-down mately 10–15 %. pressure permits proliferation of individuals adapted Our model results therefore lead us to predict that if to the novel host. a resistant allele arises in a P. oleracea population via Top-down regulation in the form of parasitism is mutation under parasitism pressure, even if that predicted to decrease the probability of adaptation due pressure decreases over time, adapted individuals are to the ‘‘challenge’’ (sensu Cox 2004) it presents to unlikely to proliferate, even in the presence of strong population growth. Population growth is important in selection presented by extensive garlic mustard cover. directional selection to offset the population size In our model we included parasitism only in the reduction from hard selection and to buffer the second generation, consistent with published data on population against drift (Reznick and Ghalambor emergence times (Benson et al. 2003). However, 2001). Enemy release reduces this challenge to parasitism rates on non-target host species are not population growth. This result is particularly intrigu- known for many parasitoids and Van Driesche (1988) ing and important in relation to native herbivore trapped C. glomerata adults in late May, indicating adaptation to exotic weeds because as noted by Harvey their presence earlier than is typically reported. If we et al. (2010b) the third trophic level is often not were to include parasitism in the first generation of our accounted for in studies of community responses to model, then the importance and negative effects of exotic weeds. Furthermore, top-down regulation is C. glomerata on P. oleracea persistence would be considered a potentially important evolutionary force greater. Our unpublished data suggest the values in our in herbivorous insect diet breadth (Dyer and Floyd model for parasitism rate are conservative. We offer 1993; Mooney et al. 2012). Based on field studies of two unpublished reports (Chew, unpublished data) of native Japanese Pieris, Ohsaki and Sato (1994, 1999) C. glomerata attacking first generation P. oleracea suggested that parasitism pressure significantly shapes larvae in forested habitats. First, a collection of *50 host usage at the population level. Enemy-free space fourth- and fifth-instar P. oleracea larvae on Card- (Jeffries and Lawton 1984) has driven host shifts and amine diphylla under beech-maple forest near Wol- expansions to novel hosts in other Lepidoptera as well, cott, VT (44°330N, 72°280W) in late June 1977 as reported in Baltimore checkerspot Euphydryas revealed[80 % had been parasitized by C. glomerata. phaeton (Bowers et al. 1992; cf. Knerl and Bowers Second, P. oleracea newly hatched (first-instar) larvae 2013), diamondback moth Plutella xylostella (Fox and placed experimentally in situ on caged Alliaria Eisenbach 1992), buckeye Junonia coenia (Camara petiolata plants on 16 May 1995, in beech-maple- 1997), and Alaskan swallowtail Papilio machaon hemlock forest near Lenox, MA (42°210N, 73°170W) aliaska (Murphy 2004). were harvested in June 1995 (Courant 1996). But some Two types of geographic variation might be cages were made from fabric with holes that were too encountered by P. oleracea that could affect adapta- large, and the dozen fifth-instar larvae were all tion to a novel host and expansion of larval diet parasitized by C. glomerata. breadth: the existence of residual genetic variation in Pieris oleracea populations declined during the butterfly populations that are fragmented in space, and nineteenth and twentieth century because of the joint the degree of enemy release. Both factors vary in the effects of habitat loss (Chew 1981) and parasitoid P. oleracea range (Benson et al. 2003; Keeler and pressure from C. glomerata (Benson et al. 2003), and Chew 2008; Van Driesche 2008, Chew, unpublished residual populations continue to be vulnerable to data) suggesting the possibility of a geographic mosaic extirpation by the butterfly’s maladaptive attraction to of evolution (cf. Thompson 1999). In populations 123 Modeling the decline and potential recovery of a native butterfly 1693 lacking adaptive variation or with strong top-down Bowden S (1979) Subspecific variation in butterflies: adaptation regulation, we expect P. oleracea populations to and dissected polymorphism in Pieris (Artogeia) (Pieri- dae). J Lepid Soc 33:77–111 decline following garlic mustard invasion. However, Bowers M, Stamp N, Collinge S (1992) Early stage of host range populations with residual variation and enemy release, expansion by a specialist herbivore, Euphydryas phaeton or enemy-free space due to other landscape factors, (Nymphalidae). Ecology 73:526–536 would be expected to be evolutionary hotspots (cf. Brodeur J, Geervliet J, Vet L (1996) The role of host spe- cies, age and defensive behavior on ovipositional Thompson 1999). decisions in a solitary specialist and gregarious gen- Gene flow among populations should magnify eralist parasitoid (Cotesia species). 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For two congeneric butterflies with smaller Chew FS (1981) Coexistence and local extinction in two pierid butterflies. Am Nat 118:655–672 geographic ranges, no successful colonization has Chew FS, Renwick JAA (1995) Host plant choice in Pieris been observed on exotic plants that attract ovipositing butterflies. In: Carde´ RT, Bell WJ (eds) Chemical females but are lethal to larvae: (a) P. virginiensis ecology of 2. Chapman & Hall, New York, oviposits on garlic mustard (Porter 1994), although pp 214–238 Chew FS, Watt WB (2006) The green-veined white (Pieris napi Courant (1996) reared two individuals to pupation on L.), its Pierine relatives, and the systematics dilemmas of garlic mustard in the field (Bowden 1971; Courant divergent character sets (Lepidoptera, Pieridae). 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