Behavioral Evolution Accompanying Host Shifts In .

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Received: 2 March 2018 Revised: 16 April 2018 Accepted: 17 April 2018DOI: 10.1002/ece3.4209ORIGINAL RESEARCHBehavioral evolution accompanying host shifts in cactophilicDrosophila larvaeJoshua M. Coleman1,2 Kyle M. Benowitz1 Alexandra G. Jost2 Luciano M. Matzkin1,3,41Department of Entomology, University ofArizona, Tucson, Arizona2Department of BiologicalSciences, University of Alabama inHuntsville, Huntsville, Alabama3BIO5 Institute, University of Arizona,Tucson, Arizona4Department of Ecology and EvolutionaryBiology, University of Arizona, Tucson,ArizonaCorrespondenceLuciano M. Matzkin, Department ofEntomology, University of Arizona, Tucson,1140 E. South Campus Drive, AZ 85721.Email: lmatzkin@email.arizona.eduFunding informationDivision of Integrative Organismal Systems,Grant/Award Number: 1557697; NationalScience FoundationAbstractFor plant utilizing insects, the shift to a novel host is generally accompanied by acomplex set of phenotypic adaptations. Many such adaptations arise in response todifferences in plant chemistry, competitive environment, or abiotic conditions. Oneless well- understood factor in the evolution of phytophagous insects is the selectiveenvironment provided by plant shape and volume. Does the physical structure of anew plant host favor certain phenotypes? Here, we use cactophilic Drosophila, whichhave colonized the necrotic tissues of cacti with dramatically different shapes andvolumes, to examine this question. Specifically, we analyzed two behavioral traits inlarvae, pupation height, and activity that we predicted might be related to the abilityto utilize variably shaped hosts. We found that populations of D. mojavensis living onlengthy columnar or barrel cactus hosts have greater activity and pupate higher in alaboratory environment than populations living on small and flat prickly pear cactuscladodes. Crosses between the most phenotypically extreme populations suggestthat the genetic architectures of these behaviors are distinct. A comparison of activity in additional cactophilic species that are specialized on small and large cactushosts shows a consistent trend. Thus, we suggest that greater motility and an associated tendency to pupate higher in the laboratory are potential larval adaptations forlife on a large plant where space is more abundant and resources may be moresparsely distributed.KEYWORDSactivity, cactophilic, Drosophila mojavensis, larval locomotion, local adaptation, plant structure,pupation1 I NTRO D U C TI O Nauthors have attributed the success of these groups to the ability of insects to rapidly colonize novel hosts (Funk & Nosil, 2008;Insects utilizing plant tissues, both living and necrotic, have under-Linnen & Farrell, 2010; Oliveira et al., 2012; Winkler & Mitter,gone one of the most successful and expansive radiations of any2008). Therefore, understanding the depth and complexity of phe-group of organisms (Bernays & Chapman, 1994; Thompson, 1968;notypic adaptations made by insects utilizing new hosts is essentialThrockmorton, 1975; Wiens, Lapoint, & Whiteman, 2015). Manyto understanding their diversity. Hypotheses for the basis of suchThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,provided the original work is properly cited. 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.Ecology and Evolution. 2018;8:6921–6931. www.ecolevol.org 6921

6922 COLEMAN et al.adaptations have largely focused around plant chemistry, and thevariation in shape, volume, and size. Among the major columnarability of insects to survive in and utilize novel chemical environ-species used, S. thurberi (utilized in Sonora) is typically the tallerments (Becerra, 1997; Ehrlich & Raven, 1964; Futuyma & Agrawal,species (4–7 m) and has numerous thick arms (15–20 cm; Gibson2009).& Horak, 1978; Turner, Bowers, & Burgess, 2005). The speciesOne ecological variable that has received considerably lessmainly utilized in Baja California, S. gummosus, is shorter (3–5 m)attention is the physical structure of the host plant, such as itswith many thinner arms (5–10 cm; Gibson & Horak, 1978; Cody,shape, volume, and more importantly the usable resource distribu-1984; Turner et al., 2005). Red barrel cactus, (F. cylindraceus), istion within the host. While adult insects are known to use aspectsshaped much differently, with a single short ( 1.5 m) but wideof plant or fruit shape as cues for oviposition on recently adapted(30–40 cm) rounded stem (McIntosh, 2002). The prickly pearhosts (Alonso- Pimentel, Korer, Nufio, & Papaj, 1998; Kanno &(O. littoralis) plant is also short ( 1 m), but consists of numerousHarris, 2000; Prokopy, 1968), it is unclear how frequently insectssmall, elliptical flat cladodes (20–30 cm long, 10–15 cm wide andhave adapted specifically to maximize fitness on plants of different2–4 cm thick) (Benson & Walkington, 1965). Other related cac-physical structure. Among the traits that potentially are influencedtophilic Drosophila species beyond D. mojavensis have colonizedby the shape, volume, and size of the host plant are the foragingadditional cactus species with variable physical characteristics.behavior of larvae. Adult foraging behavior has long been thoughtDrosophila arizonae, the sister species of D. mojavensis, is a cac-to be controlled by habitat structure (Moermond, 1979; Robinson &tus generalist throughout its range (Sonoran Desert to southernHolmes, 1982; Uetz, 1991). For insects, especially holometabolousMexico as well as the Baja California peninsula and more re-insects, host structure is unlikely to define the foraging environmentcently in southern California), occupying various species of bothfor adults, which is more likely related to the distribution of plantsprickly pear and columnar cactus (Fellows & Heed, 1972; Heed,throughout the broader landscape. However, for larvae that can only1978, 1982). Drosophila navojoa previously collected from south-crawl, the shape and volume of the host plant should present strictern Sonora and Jalisco specializes on prickly pear (O. wilcoxii) ne-boundaries to the available foraging habitat. Therefore, we hypoth-crotic cladodes and fruits (Heed, 1982). Drosophila nigrospiraculaesize that variation in the physical structure of the host plant, thatmainly utilizes the giant saguaro (Carnegiea gigantea; Fellowsis, its shape and volume, should influence larval insect behaviors re-& Heed, 1972; Heed, 1982), and cardón (Pachycereus pringlei),lated to foraging or motility.both tall cacti (12 m and 20 m, respectively) with thick stemsCactophilic Drosophila have long served as a model system for(20–40 cm and 40–150 cm, respectively) and multiple armsexamining adaptations associated with evolutionary shifts in hostpresent in the Sonoran desert (Gibson & Horak, 1978; Turnerplant usage (Matzkin, 2014). Populations of one well- studied spe-et al., 2005).cies, D. mojavensis, utilize different cactus species as hosts in fourIf the shape and volume of the necrotic cactus resources de-geographically distinct populations: prickly pear (Opuntia littora-fine the boundaries of the foraging environment for larvae, welis) on Santa Catalina Island, agria (Stenocereus gummosus) (and topredicted that movement- related behaviors should differ be-a lesser extent cochal, Myrtillocactus cochal) in Baja California, redtween flies inhabiting cacti of different shapes, and specificallybarrel cactus (Ferocactus cylindraceus) in the Mojave Desert, andthat the behavior of larvae native to larger and longer columnarorgan pipe (S. thurberi) as well as occasionally cina (S. alamosensis)cacti should reflect an ability to forage across greater distances,in the Sonoran Desert. Larval and adult D. mojavensis feed on yeastpotentially allowing access to additional or preferable sources of(Fogleman, Starmer, & Heed, 1981, 1982) and bacteria (Fogleman &nutrition. Conversely, individual larvae utilizing prickly pear clado-Foster, 1989) present in the necrotic tissues of these cacti. Cactusdes will be restricted by the size of cladode itself, limiting the needhost adaptation across these populations (reviewed in Matzkin,to travel long distances to forage.2014) have shaped variation at detoxification pathways (Matzkin,To test these predictions, we quantified pupation height and2005, 2008), life history characteristics (Etges, 1993; Etges & Heed,third- instar speed across the four D. mojavensis populations under1987; Rajpurohit, Oliveira, Etges, & Gibbs, 2013), behavior (Etges,common garden conditions. We found that flies from the CatalinaOver, De Oliveira, & Ritchie, 2006; Newby & Etges, 1998), and mor-Island population (prickly pear) were both slower and pupated closerphology (Pfeiler, Castrezana, Reed, & Markow, 2009) as well as moreto the food resource than flies from the other populations, espe-broadly at the genomic and transcriptomic (Matzkin & Markow,cially the Sonoran population (columnar). Furthermore, the specialist2013; Matzkin, Watts, Bitler, Machado, & Markow, 2006) level.species D. navojoa and D. nigrospiracula, which inhabit primarily smallFurthermore, additional closely related cactophilic species within(prickly pear) and large cactus (saguaro and cardón), respectively,the D. repleta species group have colonized variable cactus environ-display consistent results for larval speed. The generalist D. arizonaements (Oliveira et al., 2012), providing the potential for deeper evo-displays intermediate phenotypes for both pupation height andlutionary comparisons.speed. Lastly, F1 crosses between the Catalina Island and SonoranIn addition to displaying extensive chemical and microbialpopulations suggest that speed and pupation height are geneticallyvariation (Fogleman & Abril, 1990; Kircher, 1982; Starmer, 1982;independent phenotypes in D. mojavensis. We argue that both phe-Starmer & Phaff, 1983), the cactus species inhabited by D. mo-notypes are likely related to the shape, volume, and size of the hostjavensis also have striking physical differences, displaying markedcacti.

COLEMAN et al.2 M ATE R I A L S A N D M E TH O DS2.1 Experimental insectsWe utilized isofemale lines of D. mojavensis originally collected fromSanta Catalina Island, the Sonoran Desert (Organ Pipe NationalMonument, AZ), Baja California (La Paz, Mexico), and the MojaveDesert (Whitman Canyon, AZ and Anza Borrego, CA), on thecacti described above. We also used isofemale lines of the generalist species D. arizonae originally collected from Baja California(San Pedro, Mexico), Southern California (Riverside, CA), southernMexico (Hidalgo and Chiapas), and the Sonoran Desert (Tucson, AZ,Hermosillo, Mexico, and San Carlos, Mexico). Lastly, we used a multifemale stock of D. nigrospiracula collected from Saguaro (Carnegieagigantea) in Tucson, AZ, and a D. navojoa stock originally collected onprickly pear (Opuntia spp.) from Jalisco, Mexico, from the DrosophilaSpecies Stock Center (15081- 1374.11). Additional information onfly stocks and collections can be found under Dryad accessionhttps://doi.org/10.5061/dryad.j34g342. With the exception ofD. nigrospiracula, we maintained all lines on banana- molasses media(Appendix 1), at 25 C, 50% humidity, and a 14:10 light:dark cycle.Drosophila nigrospiracula was maintained on potato flake media witha necrotic saguaro homogenate mixture (Castrezana, 1997).We quantified both pupation height and larval activity inisofemale lines of each of the four D. mojavensis populations. Wemeasured pupation height from the Baja California population ofD. arizonae. We also measured larval speed in lines from four D. arizonae populations as well as D. navojoa and D. nigrospiracula. Wefurther examined both phenotypes in F1 individuals from a cross between Catalina Island (genome stock, 15081- 1352.22) and SonoranDesert (MJ122) lines. To generate F1 larvae, virgin adults werecollected from the Sonora and Catalina Island lines within 24 hr ofeclosion. Virgin females from Sonora were then crossed with virginmales from the Catalina Island population in a cage with banana agarmedium. The reciprocal cross was done in the same manner. F1 larvae were reared in the conditions described above until their use ineither pupation or activity trials.6923initial period of low activity after transfer, we utilized only the 50 sbefore each larva reached the wall of the experimental chamber(whereupon estimating the position of the larva became imprecise) for analysis. We analyzed the mean speed of each larva during this 50 sec period using the TrackMate plugin of the ImageJsoftware package (https://imagej.nih.gov/ij/). All activity trialswere performed in full light conditions, in the afternoon between12:00 and 3:00 p.m.2.3 Pupation height assaysTo measure pupation height, mated flies from stocks (see above)were maintained at low density in glass 8- dram vials with banana- molasses media and allowed to oviposit for 24 hr before being removed. Eggs were allowed another 24 hr to hatch into first instarlarvae before being collected. Using a needle, 40 newly hatched larvae were placed in fresh 95 mm tall 8- dram glass vials containing approximately 10 ml of banana- molasses medium. Vials were cappedusing a packed cotton plug (Genesee Scientific), and then incubatedat 25 C in 50% humidity on a 14:10 hr light:dark cycle. Larvae werethen allowed to develop without disturbance. Once the larvae pupated, the distance between the surface of the food and the highesttip of the pupae was measured in millimeters using a digital calliper.2.4 Statistical analysesWe analyzed pupation height data using GLMs modeled with quasipoisson error structures to account for non- normality of the data,which contained a high number of zero values. We analyzed larvalspeed data using GLMs modeled with gaussian error structures.We used Tukey’s HSD from the multcomp package (Hothorn, Bretz,& Westfall, 2008) in R to perform all pairwise post hoc comparisonsfor each GLM. We calculated Pearson’s coefficient to estimate correlations between mean pupation height and mean speed acrossisofemale lines within the D. mojavensis Catalina Island and Sonorapopulations. To assess the effects of genotype on each phenotype, weanalyzed isofemale line as a nested effect within population using thelme4 package (Bates, Mächler, Bolker, & Walker, 2015) in R. We then2.2 Larval activity assaysTo assay larval activity, we placed 7–10- day old virgin flies inused the ANOVA function to compare the performance of the mixedmodels to identical models with the nested term removed. All statistical analyses were performed in R 3.4.0 (https://www.R-project.org).mixed sex vials with the appropriate media under a 14:10- hrlight:dark cycle at 50% humidity and 25 C for 24 hr before removing all adults and allowing eggs to hatch and develop undisturbed.Upon reaching the third instar, we removed larvae from vials inrandomly selected groups of five and placed them on a 10 cm petridish partially filled with 1% agar. Larvae in the third- instar stage3 R E S U LT S3.1 Phenotypic differences across populations andspecieswere determined by body size and used irrespective of specificLarval speed varied significantly both between D. mojavensis pop-age, because species as well as the four D. mojavensis populationsulations and across species (Figure 1). Catalina Island flies werevary substantially in developmental time (Etges, 1990; J.M.C. pers.significantly slower than flies from Baja, Mojave, or Sonora. Bajaobs.). We then recorded each group of larvae for 5 min using aand Mojave populations were not different, though Sonora wasPoint Grey video camera (FLIR Systems, Wilsonville, OR, USA), anddifferent from both (Appendix 2). All populations of D. arizonaeretained images taken every 5 s. To ensure that we disregarded anlarvae displayed intermediate speeds. However, D. navojoa and

6924 COLEMAN et al.F I G U R E 1 Third- instar speed in four D. mojavensis populations, four D. arizonae populations, and single D. navojoa and D. nigrospiraculapopulations. Letters below each box indicate significant differences between species and populations. D. mojavensis–Baja n 180, CatalinaIsland n 279, Mojave n 275, Sonora n 280; D. arizonae––Baja n 196, Southern California n 35, Sonora n 463, Southern Mexicon 143; D. nigrospiracula––n 60; D. navojoa––n 108F I G U R E 2 Pupation height in fourD. mojavensis populations and oneD. arizonae population. Letters beloweach box indicate significant differencesbetween species and populations.D. mojavensis–Baja n 84; Catalina Islandn 399, Mojave n 288, Sonora n 340;D. arizonae–Sonora n 398D. nigrospiracula showed extreme phenotypes, the former beingPupation height also displayed significant variability across D. mo-slower than all but Catalina Island D. mojavensis while the latter wasjavensis populations (Figure 2). Flies from Catalina Island pupated atsignificantly faster than all other species and populations. Isofemalelower height than flies from any of the other three populations or thelines of D. mojavensis also exhibited significant genetic variationsister species D. arizonae, none of which displayed significant differ-(χ 2 256.74, p 0.0001; Appendix 3).ences in pupation height between them (Appendix 4). Isofemale lines

COLEMAN et al.6925F I G U R E 3 Third- instar speed in parental lines and F1 crossesbetween Catalina Island and Sonora populations of D. mojavensis.Letters below each box indicate significant differences betweengroups. Catalina Island n 60; Catalina Island (F) Sonora (M)n 113; Sonora (F) Catalina Island (M) n 15; Sonora n 113F I G U R E 4 Pupation height in parental lines and F1 crossesbetween Catalina Island and Sonora populations of D. mojavensis.Letters below each box indicate significant differences betweengroups. Catalina Island n 399; Catalina Island (F) Sonora (M)n 644; Sonora (F) Catalina Island (M) n 366; Sonora n 340of D. mojavensis exhibited significant genetic variability (χ 2 145.09,volume, and size of host plants or usable resource within a host plantp 0.0001; Appendix 3).(e.g., necrotic section) have seldom been investigated for their roleGenetic correlations between D. mojavensis pupation height andin creating novel selective environments for insects. For insect lar-third- instar speed were not significantly different from zero withinvae, the shape and volume of the host on which eggs are ovipos-either the Catalina Island population (r10 0.241; p 0.475) orited should constrain their movement, defining the boundaries ofwithin the Sonora population (r 9 0.203; p 0.578).3.2 Phenotypes of F1 crossestheir foraging environment. Thus, we considered larval behavioralphenotypes as strong candidates for local adaptation to plants withvariable physical characteristics. To examine this prediction, wemeasured pupation height and third- instar activity in four popula-Third- instar speed of the Sonoran population was not significantlytions of D. mojavensis, which has colonized multiple cactus host spe-different from either F1 cross, but was, as expected, greater thancies throughout southwestern North America.the Catalina Island (Figure 3). Speed of the Catalina Island popula-Larval speed was greater in D. mojavensis populations living ontion was slower than the Catalina female by Sonora male cross buttaller, larger cacti, and lowest in the Catalina Island population in-not the reciprocal. The F1 crosses were also not different from eachhabiting necrotic prickly pear cladodes. Interspecific data also sup-other (Appendix 5).port this relationship, as D. nigrospiracula specializing on the saguaroThe Sonoran population had significantly higher pupation heightsand cardón cactus have very fast larvae, while D. navojoa inhabitingthan Catalina Island flies or either F1 cross (Figure 4). Both F1 crossesprickly pear are especially

Desert (MJ122) lines. To generate F 1 larvae, virgin adults were collected from the Sonora and Catalina Island lines within 24hr of eclosion. Virgin females from Sonora were then crossed with virgin males from the Catalina Island population in a cage with banana agar medium. The reciprocal cross was done in the same manner. F 1 lar-

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