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Evolutionary Ecology ISSN 0269-7653Volume 25Number 6 Evol Ecol (2011) 25:1335-1355DOI 10.1007/s10682-011-9473-y

Rapid experimental shift in host use traitsof a polyphagous marine herbivore revealsfitness costs on alternative hosts

Erik E. Sotka & Pamela L. Reynolds

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ORI GIN AL PA PER

Rapid experimental shift in host use traitsof a polyphagous marine herbivore revealsfitness costs on alternative hosts

Erik E. Sotka • Pamela L. Reynolds

Received: 11 November 2010 / Accepted: 12 March 2011 / Published online: 27 March 2011� Springer Science+Business Media B.V. 2011

Abstract The host breadth of any particular herbivore reflects a compromise between

evolutionary forces that promote specialism and those that promote polyphagy. Because

most terrestrial herbivorous insects specialize, explorations of this evolutionary balance

have focused largely on specialist than on polyphagous herbivores. Here, we experimen-

tally tested whether fitness-based tradeoffs in utilizing alternative hosts can be detected

within a polyphagous marine herbivore. The marine amphipod Ampithoe longimana occurs

on multiple seaweeds year-round (especially the genera Sargassum, Ulva and Hypnea), but

is particularly abundant on the diterpene-rich genus Dictyota during warmer summer

months. If fitness-based tradeoffs in using these alternative hosts are present, A. longimanamay experience fluctuating selection across seasons. To test this possibility, we performed

a controlled natural-selection experiment in which amphipods were isolated on Dictyota or

a mixed seaweed assemblage that did not include Dictyota. Within 15 weeks (less than five

overlapping generations), Dictyota-lines had greater feeding tolerance for Dictyota and its

secondary metabolites than did mixed-seaweed-lines. Dictyota-line females reproduced

more quickly than did mixed-seaweed-line females on Dictyota, but mixed-seaweed-line

juveniles had greater growth on Sargassum and Ulva and higher fecundity on all hosts than

did Dictyota-line juveniles. While experimental shifts in preference and performance are

likely genetically-mediated, our experimental protocol does not preclude a role for phe-

notypic plasticity. The presence of a fitness cost to evolving greater preference for Dictyotasuggests that fluctuating selection may operate on feeding preference across seasons, but

E. E. Sotka (&)Department of Biology and Grice Marine Laboratory, College of Charleston, 205 Fort Johnson Road,Charleston, SC 29412, USAe-mail: [email protected]

P. L. ReynoldsDepartment of Biology, University of North Carolina, Chapel Hill, NC, USAe-mail: [email protected]

Present Address:P. L. ReynoldsThe College of William and Mary, Virginia Institute of Marine Science, 1208 Greate Road, GloucesterPoint, VA 23062-1346, USA

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Evol Ecol (2011) 25:1335–1355DOI 10.1007/s10682-011-9473-y

Author's personal copy

our test of this hypothesis was equivocal. We suggest that one reason that polyphagy

persists within A. longimana and potentially other marine grazers is because polyphagy

broadens resource use across seasons, and this benefit outweighs the fitness-based costs

that can favor specialism. Our results also reinforce the notion that timescales of ecological

and evolutionary dynamics can overlap.

Keywords Controlled natural selection experiment � Marine plant-herbivore

interactions � Secondary metabolite � Trade-offs � Herbivore tolerance

Introduction

The evolutionary mechanisms that sculpt the host breadth of herbivores are complex and

have proven vexing to disentangle (Futuyma and Moreno 1988; Jaenike 1990; Schoo-

nhoven et al. 2005; Strauss and Zangerl 2002; Tilmon 2008), but one parsimonious view is

that the breadth of any particular herbivore reflects a ‘compromise’ (Rausher 1992)

between evolutionary forces that promote specialism versus generalism. If true, then a

complete understanding of host breadth requires biologists to simultaneously evaluate the

strength of multiple forces (e.g., host availability, food quality, and predator or abiotic

refuge) across the tremendous diversity of herbivores and their feeding strategies.

Because most terrestrial herbivorous insects utilize a restricted number of plant families

as hosts (Bernays and Graham 1988; Strong et al. 1984), it is not surprising that this

literature is dominated by studies on specialists. In contrast, the evolutionary ecology of

small polyphagous herbivores has been relatively neglected, despite the sizable number of

known polyphagous insects (root-feeding insects, grasshoppers and some lepidopterans:

Bernays and Minkenberg 1997; Novotny and Basset 2005; Novotny et al. 2002; Singer

2008; Wiklund and Friberg 2009) and the profound impacts of some of these generalists on

the population dynamics and fitness of their hosts (Price 2003).

One of the important differences between generalist and specialist insects is their response

to seasonal variation in the quantity and quality of favored host plants. Specialists tend to

emerge when the young, more nutritious foliage of favored host plants become available

(Cates 1980; Novotny and Basset 1998; Wolda 1988). In contrast, many (but not all)

polyphagous herbivores reproduce year-round and are thus forced to shift hosts across

seasons either because favored host plants are unavailable or of poor food quality. These host

shifts are largely assumed to be phenotypic, but there remains the untested possibility that the

shift may reflect fluctuating selection for alternative hosts. This could occur when popula-

tions of a short-lived herbivore adapted to summer hosts during the summer, to winter hosts

during the winter, or both. To our knowledge, the possibility of seasonal genetic response has

not been addressed for any herbivore. The distinction between a plastic and temporal genetic

response is important, because both would yield generalism at the population level (Kassen

2002; Levins 1968), but through very different evolutionary mechanisms.

Marine plant-herbivore interactions allow biologists to test ecological and evolutionary

hypotheses that were developed from terrestrial plant-insect interactions and using taxa

that are phylogenetically independent (e.g., Amsler and Fairhead 2006; Hay and Steinberg

1992; Jormalainen and Honkanen 2008; Paul et al. 2001; Sotka et al. 2009). One prominent

group of marine herbivores is amphipods (Crustacea), which are proposed by Hay et al.

(1987) as ‘‘insect equivalents’’ due to a number of shared traits: (1) insects and amphipods

are small relative to the physical size of their host plants, (2) both taxa utilize their host

plants as food and habitat, and (3) both can have large impacts on host community

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structure when released from consumption by enemies (Davenport and Anderson 2007;

Duffy and Hay 2000; but see Poore et al. 2009; Tegner and Dayton 1987).

Most herbivorous amphipods are polyphagous. Approximately 60% of amphipod spe-

cies in the herbivorous family Ampithoidae (hereafter, amphipods) can be found on two or

more orders of seaweeds (Poore et al. 2008), a rate of specialization that is comparable to

that for tropical root-feeding insects (Novotny and Basset 2005). Amphipods are unable to

diapause and cannot emerge when preferred hosts are available (as many specialist insects

do). This has led to the hypothesis that amphipod polyphagy is favored evolutionarily

because preferred hosts are unavailable during some seasons, thus forcing amphipods onto

other hosts (Hay and Steinberg 1992; Steneck and Watling 1982). While it is clear that

marine herbivores respond to seasonal shifts in host availability by altering their diets in a

phenotypically-plastic manner (Cannicci et al. 2007; Clements and Choat 1993; Kotta et al.

2006), to our knowledge, there are no published studies that looked for a seasonal genetic

response to the seasonality of algal availability (i.e., fluctuating selection) or the evolu-

tionary potential for a genetic response.

Ampithoe longimana study system

The amphipod Ampithoe longimana is an abundant herbivore within high-salinity estu-

aries from Nova Scotia to Florida. It utilizes seagrasses (Nelson 1980) and at least 25

genera within 13 orders from all macroalgal phyla as hosts (Brooks and Bell 2001; Duffy

1989; McCarty 2008). Dispersal among hosts in A. longimana has not been assessed, but

given that other ampithoid amphipods are not isolated to a single host plant (Poore 2004),

it is likely that A. longimana are individually polyphagous. In North Carolina, the

amphipod is particularly abundant on seaweeds in the tropical genus Dictyota during the

warmer summer months (Duffy and Hay 1994). This host provides refuge from predation

by omnivorous pinfish, which voraciously consume most non-Dictyota seaweeds but

avoid Dictyota and its diterpene alcohols (Duffy and Hay (1991, 1994). However,

Dictyota is unavailable during the colder winter and spring months (Richardson 1979)

(Fig. 1). Although Ampithoe longimana is found on other seaweeds year-round (Sar-gassum, Ulva, Hypnea, Gracilaria), these hosts are likely to be particularly important

during the winter and spring when Dictyota is unavailable. Because amphipods produce

offspring year-round (time to 1st reproduction is 14–21 days; Cruz-Rivera and Hay 2001;

Nelson 1980; Sotka and Hay 2002), it is possible that A. longimana is subject to fluc-

tuating selection across seasons for alternative hosts (i.e., use of Dictyota during warmer

months and of other seaweeds during colder months) if there are tradeoffs in using these

alternative hosts.

We used a controlled natural-selection experiment (Fry 2003) to test whether fluctuating

selection could potentially shape A. longimana host use. We mimicked seasonal field

distributions by isolating amphipods on Dictyota species (Dictyota-line) or a mix of

common seaweeds without Dictyota (mixed-seaweed-line) for 15 weeks. Feeding prefer-

ence and juvenile performance assays addressed the following questions: (1) Does

amphipod feeding preference for Dictyota differ between Dictyota-lines and mixed-sea-

weed-lines? (2) Are these differences mediated by the lipophilic secondary metabolites

produced by Dictyota? (3) Does fitness (survivorship, growth, reproduction) of juveniles

differ across experimental lines when confronted with Dictyota versus other foods? The

tradeoff hypothesis predicts that the reaction norms of fitness when reared on alternative

foods will cross across experimental lineages (Fry 1996). (4) Among field-collected

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amphipods, does the feeding preference for Dictyota vary among seasons? The fluctuating

selection hypothesis predicts that A. longimana populations will have greater affinity for

Dictyota at the end of summer compared to populations collected at the end of winter.

Materials and methods

Collection of organisms

All seaweeds (Sargassum filipendula, Dictyota menstrualis, D. ciliolata, Gracilariaverrucosa, Hypnea musciformis, Ulva lactuca and U. intestinalis) were collected from

shallower than 2.0 m below MLLW within seagrass, jetty and mudflat habitats in Bogue

Sound, North Carolina (34�410 N, 76�410 W). We returned seaweeds within 2 h of col-

lection to running seawater tables at the University of North Carolina’s Institute of Marine

Sciences in Morehead City, NC. Within 24 h, seaweeds were rinsed, cleaned of all epi-

biota and were either flash frozen on dry ice or added fresh to experiments. Frozen

seaweed tissue was returned to the College of Charleston’s Grice Marine Laboratory in

Charleston, South Carolina, lyophilized, ground into a fine powder using a Wiley mini-

mill, and stored at -20�C until use. Previous work indicates that lyophilization maintains

concentrations of some lipophilic metabolites such as diterpenes (Cronin et al. 1995) and

does not substantially lessen the ability of seaweeds with known lipophilic deterrents to

reduce consumer feeding rates (Bolser and Hay 1996; Cruz-Rivera and Hay 2001). Using

lyophilized seaweeds ensures that the same tissues are offered to all A. longimana at all

time points and there are no temporal changes in seaweed quality. Moreover, for A.longimana and the seaweeds used here (Sargassum, Dictyota and Ulva), the ranking of

feeding preference is similar regardless of whether amphipods are offered fresh or

lyophilized seaweed tissue (Duffy and Hay 1991; Sotka, unpublished data), suggesting that

morphological aspects are less important than nutritional or chemical defenses in deter-

mining seaweed palatability.

To seed the selection experiment, female Ampithoe longimana were collected in June

2008 from the seaweeds listed above plus Ectocarpus spp. We did not assay the feeding

preferences of these females prior to their introduction into the experiment although overall

initial preferences across cultures is likely to be similar as amphipods from multiple

sources were mixed thoroughly before allocation to the replicate lines.

Fig. 1 Seawater temperatures(max to min) within BogueSound, North Carolina fromJanuary to December. Among themost important host plants for theamphipod Ampithoe longimanaare tropical seaweeds in thegenus Dictyota, which is foundabundantly (black bar) andintermittently (grey bars) duringwarmer months. Subtidal datarecorded at Rachel CarsonNational Estuarine ResearchReserve during 2004 (34.708N;76.628W; http://nerrs.noaa.gov/)

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http://nerrs.noaa.gov/

Controlled natural selection experiment

Three replicate cultures were isolated with mostly Dictyota menstrualis and some D.ciliolata (=Dictyota-line), while six replicate cultures were isolated with a mix of seaweeds

from several divisions (= mixed-seaweed-line; S. filipendula, G. verrucosa, H. musciformisand U. lactuca). Approximately 50 pregnant females were placed into each of nine plastic

tubs that contained * 4L of aerated seawater (30–32 ppt; 25�–28�C) and exposed to full

spectrum aquarium lights (T-5 fluorescent lighting bulbs; Ushio, Tokyo, Japan) at a 12:12

(day: night) cycle and to natural light from nearby windows. Field-collected females tend

to produce between 5 and 20 juveniles, and we estimate that the initial starting density was

between 250 and 1,000 amphipods per replicate tub. Females plus their juveniles were

allowed to consume U. intestinalis for 7 days before the treatment seaweeds were added.

Ulva intestinalis was chosen as an initial base diet when establishing the experimental

cultures because it is a readily-available, high-quality food that has no known secondary

metabolites. Prior to addition to the cultures, all seaweed was dipped twice in freshwater

for 30s to remove amphipods and robustly shaken to remove snails and other epibionts.

Seawater was replaced every 1–2 weeks, and seaweeds were replenished as needed (once

or twice per week).

We did not quantify the population sizes within these cultures, although the numbers

were likely on the order of 100s rather than 1,000s per replicate tub. Thus, we cannot

eliminate the possibility that genetic drift played a role in the evolution of host use traits,

although this possibility seems unlikely given the consistency of the feeding preferences

across independent lines (see Results). We did not create discrete generations (i.e., remove

adults after they had reproduced), and therefore our experimental selection is constrained

by the presence of overlapping generations. We do not have good estimates of longevity of

A. longimana, but we have generally seen 6–8 weeks in the laboratory (personal obser-

vation). Field-based estimates of longevity in other ampithoids is on the order of months

(Sainte-Marie 1991). Because amphipods become fecund after approximately 2–3 weeks

on high quality diets at 20–25�C (Cruz-Rivera and Hay 2001; Sotka et al. 2003), our

15-week experiment likely represents between two and five generations.

We generated twice as many mixed-seaweed replicates than Dictyota-line replicates

because we initially intended to compare the evolutionary response of amphipods in the

presence and absence of cues from predatory pinfish cues. However, we failed to detect

consistent differences in feeding preference between amphipods from fish-cue vs. no-fish-

cue treatments (data not shown) and therefore analyzed both sets of lines as mixed-

seaweed-lines. We assayed between two and five cultures per treatment type each week

and made adjustment for unequal sample sizes in subgroups using a Satterwaite approx-

imation (following Sokal and Rohlf 1981).

Feeding choice assays

We assessed changes in feeding preference using laboratory-based feeding choice assays in

which amphipods were offered a choice between freeze-dried tissue from a single Dictyotaspecies and Ulva intestinalis. Freeze-dried seaweeds were embedded within agar and

bound onto window screen (for recipe see Sotka and Giddens 2009). This procedure

created two grids (i.e., 6 9 5 squares of each type of food) to quantify consumption.

Individual replicates were terminated and measured after consumption of at least 10 total

squares to ensure amphipods had fed enough to demonstrate feeding preferences. We

disregarded replicates in which all of one grid and at least half of another grid were

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consumed to prevent skewing of preferences due to reduced availability of one food type.

Assays generally lasted less than 2 days, but no longer than 5 days. The mean replicate

size per feeding assay per replicate line was 16 (standard error = 1.1) and the number of

total squares consumed averaged 20.0 (standard error = 0.4).

For each replicate amphipod assay, we calculated the proportion of Dictyota tissue

consumed using the ratio: (Number of squares of Dictyota consumed) 9 (Total # of

squares consumed)-1. These values were then assessed statistically using nonparametric

ANOVAs, where statistical significance was evaluated by comparing F-ratios with an

expected distribution generated from 1,000 permutations of the dataset (Anderson 2001)

using R (http://cran.r-project.org). The non-parametric approach is appropriate because the

data are not normally distributed and could not be transformed to yield normality, and

because all replicates are independent and exchangeable. We pursued a one-way non-

parametric ANOVA that nested the effect of replicate culture within treatment. We also

pursued a one-way nonparametric ANOVA in order to assess the effect of season on

feeding preference, and used a series of pairwise nonparametric ANOVAs for post hoc

analysis. We also assessed for the final week of assays of D. menstrualis (Week 19) the

relative consumption of Ulva and D. menstrualis using a paired t-test.

We offered amphipods a feeding choice between U. intestinalis tissues coated with or

without lipophilic metabolites from Dictyota ciliolata. Plants were collected from Radio

Island Jetty in June 2008, flash-frozen on dry ice, lyophilized, milled and stored at -20�C.

In October 2008, six grams of dried tissue were extracted thrice for 30 min in a total of

180-mL of 1:1 ethyl acetate:methanol. The extract was Whatman-disc filtered and rotary-

evaporated to remove solvents. The extract was then dissolved in 20-mL of ethyl acetate,

added to freeze-dried U. intestinalis, and rotary-evaporated. To create control foods,

20-mL of ethyl acetate was added to freeze-dried U. intestinalis and rotary-evaporated.This assay was designed and analysed as a nested ANOVA, with replicate (n = 8–11) tubs

within each treatment type.

Performance assays

We assessed the fitness of amphipods by rearing juveniles collected from experimental

females at week 15. Females were collected from each of the two sets of lines, and offered

fresh Ulva intestinalis for 1 week. Females were collected haphazardly across all cultures

(tubs) but we did not record tub origin for each female. Four emerged juveniles from each

of thirty females were isolated with one of four food treatments (no food, fresh tissue of

Dictyota menstrualis, Sargassum filipendula or Ulva intestinalis) within individual 40-mL

Petri dishes. We maintained the experiment at room temperature, changed seawater and

foods every 3–4 days, and checked for mortality and female maturity every 1–2 days.

Antibiotics (100 mg/mL each of streptomycin and penicillin) were dissolved into seawater

collected from Bogue Sound, NC in order to minimize bacterial infection in our assay. At

the end of 25 days, surviving amphipods were digitally photographed and body length

determined using Image-J.

All animals isolated with no food died within 4 days. For the survivors, we used

parametric survival curve analysis to assess survivorship curves and age to maturity (which

combines days to reproduction with the overall proportion of females that became

reproductive). Because all juveniles from replicate lines were grouped together, we cannot

estimate variation in these parameters. Growth rates and female fecundity were assessed

via a series of nonparametric ANOVA similar to those described for feeding assays above.

Because the results indicated that the selected lines shifted their life-history strategies

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http://cran.r-project.org

(see Results), we directly compared the relative contribution of survivorship, number of

eggs produced, and age at maturity in a single estimate of population rate of intrinsic

capacity (rC) following Southwood (1978), which is a proxy for intrinsic rate of population

increase. The estimate of population growth rate does not account for multiple broods nor

longevity of the amphipods. To assess whether rC estimates were significantly different, we

performed bootstrap analysis following Meyer et al. (1986). Individuals were sampled

(with replacment) 1,000 times per treatment combination (e.g., Dictyota-line on Dictyota),

and estimates of mean rC and their 95% confidence intervals were calculated via Equa-

tion 3 of Meyer et al. (1986).

Temporal and spatial variation in feeding preference

In order to assess temporal variation in feeding preference, A. longimana were collected in

November 2008 and May and October 2009, and May and November 2010 from Sar-gassum filipendula in Bogue Sound. In order to minimize the effect of recent feeding

history on feeding preferences (Poore and Hill 2006), individuals were initially fed for

3 days on only Ulva intestinalis before we initiated the feeding choice experiment. We

also collected amphipods from alternative hosts (Dictyota vs. Hypena, and Dictyota vs.

Sargassum) to test for the presence of sympatric host races. To compare the feeding

preferences of A. longimana collected on alternative host sources (e.g., Dicytota vs.

Hypnea), we used a paired t-test to compare feeding rates on the two seaweeds and an

unpaired t-test to compare the relative consumption of D. menstrualis between amphipod

sources.

Results

Experimental shift in feeding preference

Experimental shift of adult feeding preferences occurred within 15 weeks (Fig. 2a). During

the early stages of the experiment (Week 7), adults from Dictyota-lines and mixed-sea-

weed-lines did not significantly differ in their relative preference for Dictyota because of

significant variance among replicate lines within treatments (Table 1). By the end of Week

12 (estimated at between two to five overlapping generations), adults from Dictyota-lines

consumed significantly more D. menstrualis than did adults from mixed-seaweed-lines,

and within-treatment variance was nonsignificant.

To minimize the role of recent feeding history, we placed all lines onto a mixed

seaweed diet for 2 weeks and then re-evaluated feeding preference for Dictyota men-strualis. A set of paired t-tests found that Dictyota-lines consumed slightly more D.menstrualis than Ulva (Fig. 2a; t = 2.059, n = 46, P = 0.043) while mixed-seaweed-lines

consumed significantly more Ulva than D. menstrualis. (t = -2.76, n = 40, P = 0.007).

A direct test of relative consumption of Dictyota indicates that although adults from

Dictyota-lines did not feed on Dictyota as readily after this ‘relaxation’ period, the adults

maintained a greater feeding preference for D. menstrualis relative to adults from the

mixed-seaweed lines (Fig. 2a; Table 1).

We also document an experimental shift of feeding preference for Dictyota ciliolata.

Dictyota-lines consumed more D. ciliolata than did mixed-seaweed-lines at weeks 12 and

15 (Fig. 2a; Table 1). As has been seen repeatedly with these amphipods (Cruz-Rivera and

Hay 2003; Duffy and Hay 1991; Sotka and Hay 2002), feeding preferences for Dictyota

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species are mediated by lipophilic metabolites, including diterpene alcohols. When offered

a feeding choice between control and extract-coated foods at Week 15, Dictyota-lines

consumed twice as much extract-coated tissue than did the mixed-seaweed-lines (Fig. 2c;

Table 1).

Fitness tradeoffs in using alternative seaweeds

The experimental shift in host use revealed the presence of fitness-based tradeoffs when

utilizing alternative seaweeds. At the end of week 15, we removed females from experi-

mental lines and isolated their juveniles on three seaweed diets (Dictyota menstrualis,

Sargassum filipendula, and Ulva intestinals) and measured diet- and lineage-specific rates

of survivorship, growth and reproduction. Survivorship did not significantly differ among

amphipod lines, neither when compared on a single diet (analyses not shown) nor when all

diets were combined (v2 = 1.99; P = 0.160; Fig. 3a). The growth rate of juveniles from

mixed-seaweed-lines was faster than those of Dictyota-lines when all diets were combined

Fig. 2 Changes in feeding preferences during a controlled natural-selection experiment. Relative feedingpreference (mean ± S.E.) for (a) Dictyota menstrualis (b) D. ciliolata and (c) the lipophilic extract of D.ciliolata within paired-choice feeding assays is plotted for each amphipod line. Amphipod lines wereisolated on Dictyota species (‘Dictyota-lines’) or a mix of other seaweeds (‘Mixed-seaweed-lines’) for15 weeks. All cultures were placed onto a mixed seaweed diet on week 16 (see arrow). Points connected bylines indicate results from individual selection lines. See Table 1 for statistical details

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(Fig. 3b). Growth also varied across diet (Ulva [ Dictyota [ Sargassum), but an inter-

action between diet and lineage was not significant. Mixed-seaweed-lines produced a

greater number of eggs than did Dictyota-lines when animals from all diets were combined

(Fig. 3c; Table 2). When reared on Dictyota, Dictyota-line females became reproductive

more quickly compared to the mixed-seaweed females (Fig. 3d; v2 = 4.87; P = 0.027).

There was no difference among lines in time to female reproduction when reared on

Sargassum (v2 = 0.64; P = 0.420) or Ulva (v2 = 0.21; P = 0.650; Fig. 3d).

Table 1 ANOVAs from feeding preference assays in Fig. 2

D.f. M.S. F P

Relative consumption of Dictyota menstrualis

Week 7

Treatment 1 0.912 1.708 0.273

Culture {Treatment} 3.4 0.534 2.872 0.019

Error 85 0.111

Week 12

Treatment 1 3.064 26.859 0.008


Error 85 0.085

Week 15

Treatment 1 7.938 47.617 0.002

Culture {Treatment} 4 0.167 1.984 0.100

Error 137 0.084

Relaxation

Treatment 1 0.878 199.015 \0.001


Error 80 0.068

Relative consumption of D. ciliolata

Week 12

Treatment 1 2.417 50.331 0.003


Error 87 0.046

Week 15

Treatment 1 3.341 37.742 0.005


Error 139 0.138

Relative consumption of D. ciliolata extract

Week 15

Treatment 1 2.089 19.311 0.016


Error 47 0.106

Treatment indicates two types of selection lines (Dictyota-lines vs. Mixed seaweed-lines). Between two andfive cultures are nested within each treatment type

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Thus, the mixed-seaweed-lines tended to grow more quickly (Fig. 3b) and their females

produced more eggs (Fig. 3c) relative to the Dictyota-lines, but the Dictyota-lines became

fecund more quickly on Dictyota (an average of 3.4 days earlier; 15.0 vs. 18.4 days;

Fig. 3d). In order to reconcile these life-history patterns, we summarized survivorship, age

to maturity, and female fecundity into a simplified metric, the intrinsic rate of population

increase (or rC). There is a clear qualitative shift among lineages in the hierarchical rank of

diets that provide the greatest population growth: Dictyota provided Dictyota-lines with the

greatest rC, while Ulva intestinalis provided the greatest rC for the mixed-seaweed lines.Both sets of experimental lineages had their lowest rC on Sargassum filipendula (Fig. 3e).

Testing predictions using field-collected amphipods

The rapid evolution of host use traits for alternative seaweeds (Fig. 2), in combination with

the presence of an apparent tradeoff in using alternative hosts (especially for female time to

maturity; Fig. 3d) yields two predictions. The first is that individuals collected from

Dictyota or alternative hosts differ substantially in host use traits by either genetic or

phenotypic mechanisms. There was no significant difference in the willingness of Dict-yota- or Sargassum-collected amphipods to consume these seaweeds (Fig. 4a; unpaired

t-test P = 0.803). There was also no significant difference among Dictyota- or Hypnea-

collected amphipods to consume these seaweeds (Fig. 4b; unpaired t-test P = 0.113).

The second prediction is that feeding preference in field-collected populations may shift

seasonally due to fluctuating selection. That is, amphipods collected when Dictyota has

been abundant (i.e., fall) should be more willing to consume Dictyota compared to am-

phipods collected when Dictyota is absent (i.e., spring). When offered a feeding choice

between freeze-dried tissue from Dictyota menstrualis and Ulva intestinalis, A. longimanacollected in November-2008 (at the end of fall) consumed nearly twice as much Dictyotatissue as A. longimana collected in May-2009 (at the end of winter) (Fig. 4c). However,

amphipods collected in October-2009 did not differ from amphipods collected in May-

2009, June-2010 nor October 2010. Thus, if there is fluctuating selection on Dictyotausage, then its effectiveness varies across years. It is unlikely these patterns are driven by

their recent history, as all amphipods were collected from a mix of non-Dictyota seaweeds

(e.g., Sargassum and Hypnea) and fed on Ulva intestinalis for at least 3 days prior to

feeding assays, although there remains the possibility of effects of previous diet that linger

for more than 3 days.

Table 2 ANOVAs from amphi-pod size and number of eggs(Fig. 3b–c). Treatment indicatestwo types of selection lines(Dictyota-lines vs. Mixed sea-weed-lines). Diet was eitherSargassum, Dictyota or Ulva

D.f. M.S. F P

Final size of amphipods

Treatment 1 2.393 4.730 0.035

Diet 2 10.932 20.546 \0.001

Treatment 9 Diet 2 0.832 1.644 0.177

Error 86 0.506

Number of eggs

Treatment 1 8.787 4.193 0.047

Diet 2 2.063 0.984 0.407

Treatment 9 Diet 2 0.146 0.0695 0.930

Error 33 2.096

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Fig. 3 Fitness of amphipods from the controlled natural-selection experiment. Amphipods from two typesof selection lines (Dictyota- or mixed-seaweed lines) were reared for 25 days on three diets (n = 29;Dictyota menstrualis, Ulva intestinalis and Sargassum filipendula). a Survivorship, b body size (n = 13–17;see Table 2 for statistical details), c female fecundity (n = 3–9; see Table 2 for statistical details) andd female age to maturity are indicated. The asterisk in d refers to a significantly faster maturity rate ofDictyota- than of mixed-seaweed females when reared on Dictyota. e Survivorship, age to maturity, andfecundity were used to estimate the capacity of increase (rC) and its 99% confidence intervals. Lettersindicate significant differences as detected by confidence intervals (Meyer et al. 1986)

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Discussion

The host breadth of any particular herbivore reflects a ‘compromise’ (Rausher 1992)

between evolutionary forces that promote specialism and those that promote generalism.

Because most terrestrial herbivorous insects specialize (Bernays and Graham 1988; Strong

et al. 1984), we have a clearer sense of this evolutionary balance for specialist than for

polyphagous herbivores, either marine or terrestrial (see Introduction). Here, we experi-

mentally addressed the evolution of feeding preference in the polyphagous herbivore

Ampithoe longimana. One principal finding is that within a few months of a controlled

natural-selection experiment, lines isolated on Dictyota displayed greater feeding tolerance

for Dictyota and its secondary metabolites compared to lines isolated on alternative hosts

(Sargassum, Hypnea, and Ulva; Fig. 2).

Fig. 4 The feeding preferences of amphipods collected from field-collected amphipods. a Dictyota-collected and Sargassum-collected amphipods were offered a choice of freeze-dried Dictyota menstrualisand Ulva intestinalis during August 2009. Mean (±S.E.) consumption of tissues during the assay arepresented. b Dictyota-collected and Hypnea-collected amphipods were offered a choice of fresh tissue ofDicytota menstrualis and Hypnea musciformis during July 1999. An asterisk indicates a significant(P \ 0.05) paired t test when comparing consumption of the alternative seaweeds. Mean (±S.E.)consumption of tissues during the assay are presented. c Relative consumption (Mean % Dicyota ± S.E.) offreeze-dried Dictyota menstrualis of amphipods collected in the fall and spring. Treatments that share aletter are statistically indistinguishable by Tukey–Kramer posthoc

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The shift in feeding preferences likely reflects evolution because non-genetic expla-

nations are less compelling for several reasons. First, feeding preference for Dictyota is a

heritable, autosomal trait (Sotka 2003; Sotka et al. 2003). Second, we forced individuals

to all consume the same food (Ulva intestinalis) for several days before assays began,

minimizing the effects of recent feeding history. Third, even after we allowed all lines to

consume the mixed-seaweed diet for 2 weeks, Dictyota-lines continued to consume

relatively more D. menstrualis than did the mixed-seaweed-lines (See week 19; Fig. 2a).Fourth, when amphipods were collected in the field from Dictyota versus alternative

hosts (Sargassum or Hypnea), host type did not significantly predict the willingness to

consume Dictyota (Fig. 4a, b). Finally, the patterns of feeding preference by adults for

Dictyota versus Ulva mirrored the relative performance of offspring on those foods.

Specifically, Dictyota-line adults only weakly preferred Dictyota to Ulva in feeding

choice assays (Fig. 2a at week 19), and their performance was equivalent on the two

seaweeds (as measured by the intrinisic rate of growth; Fig. 3e). In contrast, mixed-

seaweed-line adults significantly preferred Ulva over Dictyota (Fig. 2a) and their off-

spring also had greater performance on Ulva than Dictyota. Given that these offspring

were reared outside the experimental treatments and thus were naıve to either food, these

patterns suggest that both performance and preference differences across lineages have a

genetic component.

While these lines of evidence indicate that shifts in feeding preference are likely

genetic, our experimental protocol does not preclude a role for phenotypic plasticity. To

ensure that feeding preferences and performance patterns were genetically-mediated,

amphipods would need to be reared on a uniform food source for at least two generations

after selection occurred. Thus, our observed feeding patterns (Figs. 2 and 4) and perfor-

mance tradeoffs (Fig. 3) could be have been mediated by feeding experiences of young

juveniles or epigenetic cues inherited from mothers. Genetically-mediated differences

among individuals in feeding preference and plastic responses would both yield gener-

alism at the population level (Kassen 2002; Levins 1968), but through different

mechanisms.

Presence of a performance cost

Our experiment also suggests fitness consequences of adapting to alternative hosts.

Dictyota-line females become reproductive more quickly when on Dictyota than did

mixed-seaweed-line females (Fig. 3d). In contrast, when isolated on Sargassum and Ulva,

mixed-seaweed-lines grew more quickly and produced more eggs than did Dictyota-line

individuals (Fig. 3a–c). These patterns suggest there is a cost to adapting to Dictyotawhen isolated on non-Dictyota seaweeds. The observed cost does not appear to be

symmetrical; that is, a greater cost is incurred when Dictyota-adapted individuals are

isolated on non-Dictyota species, compared to when mixed-seaweed-lines are isolated on

Dictyota. While fitness costs do not necessarily indicate a formal tradeoff because our

reaction norms do not cross, the presence of fitness costs to evolving greater preference

for Dictyota are strong enough in theory to drive the evolution of specialist feeding

preferences for Dictyota (Fry 1996). One caveat to these conclusions is that because we

haphazardly sampled females from across experimental cultures, we cannot statistically

assess the relative strength of between-culture and between-treatment variation in

performance.

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These laboratory-based estimates of fitness are mediated by food quality and as such, do

not address whether amphipod fitness is altered by extrinsic plant traits (i.e., abiotic stress,

mate encounter success, or predation refuge). In this system, there is reason to suspect

that field conditions will amplify observed tradeoffs. Specifically, earlier maturation of

females from Dictyota-lines compared to females from mixed-seaweed-lineages when on

Dictyota (a 3 day difference) (Fig. 3d) may be highly and ecologically relevant. We have

no empirical estimates of predation rates of A. longimana on Dictyota in the field, but

presumably the delayed maturity of mixed-seaweed-lines on Dictyota would make those

genotypes more susceptible to predation than Dictyota-lines (Duffy and Hay 1994). If true,

then the cost of adapting to a mixed-seaweed assemblage may be greater in the field than is

apparent in our laboratory-based assays. Whether fitness tradeoffs are mediated by genetic

or phenotypic mechanisms, the ecological interactions with predators would be function-

ally similar.

The presence of fitness costs in A. longimana mirrors a growing list of fitness-tradeoffs

in other seaweed-herbivore interactions. Molluscan herbivores (snails and slugs) produce

radular types that differ in their effectiveness when grazing particular seaweeds (Steneck

and Watling 1982), and tradeoffs arise when a mismatch between radular type and the

available seaweed occurs (Padilla 1985; Trowbridge 1991). Other mollusks are apparently

susceptible to analogous mismatches in other herbivore traits (e.g., ‘suction pressure,

salivary enzyme or feeding methods’ (Trowbridge and Todd 2001)). The isopod Idoteabalthica also displays tradeoffs: individuals collected from the brown seaweed Fucusvesiculosus grew faster on Fucus than did individuals collected from seagrass Zosteramarina, and vice versa (Vesakoski et al. 2009).

The growing number of tradeoffs found within polyphagous herbivores (including

terrestrial insects; Singer 2008) remains paradoxical given that tradeoffs tend to favor the

evolution of specialization. One resolution of this conflict is that the benefit of using

multiple hosts (i.e., broadening the resource base) may outweigh its fitness cost (Poore

et al. 2008). Polyphagy in A. longimana appears to be favored because it broadens resource

use across seasons, and this benefit outweighs the fitness-based costs that favor the evo-

lution of specialism on Dictyota. As a contrasting example, the isopod Idotea balthicaspecializes on the brown seaweed genus Fucus (Jormalainen et al. 2001) despite the fact

that Fucus is a relatively poor quality food for Idotea juveniles relative to alternative hosts.

However, Fucus can be found year-round while those alternative foods largely disappear

during colder winter months. Thus, A. longimana is a generalist that uses the seasonally

available Dictyota as one of a suite of species, while Idotea is a specialist on the con-

sistently-available Fucus. For these herbivores, the temporal variability of host plants and

host breadth are positively related, a hypothesis that has broad theoretical (Levins 1968)

and empirical support (Cates 1981; Jaenike 1978, 1990; Kassen 2002; Wiklund and Friberg

2009; but see Futuyma 1976).

Equivocal evidence for fluctuating selection

Because this amphipod can evolve host use traits rapidly (within a few months), it is

possible that feeding preference for Dictyota may evolve seasonally via fluctuating

selection. Indeed, individuals collected in November-2008 (after the warm summer)

showed greater feeding preference for Dictyota than did individuals collected in May-2009

(after the cold winter; Fig. 4c). However, feeding preference did not differ between spring

and fall collections in 2009 nor 2010, across which we would have expected an increase in

1348 Evol Ecol (2011) 25:1335–1355

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feeding preference for Dictyota. There are several possible explanations for the lack of a

field response during the summer of 2009 and 2010. First, any signal of fluctuating

selection would require that Dictyota-adapted individuals would disperse from Dictyotaplants onto Sargassum and such effective dispersal may differ between years. Second,

selection to utilize Dictyota may not have been as effective during the summer of 2009

relative to the summer of 2008. Third, the field pattern may reflect genetic drift, inade-

quately-sampled populations, or both. Resolving these alternatives will require assaying

amphipod feeding preferences over a number of years, and rearing those amphipods within

a common garden environment for a full generation in order to minimize environmental

and maternal effects.

Implications of rapid evolution

If the shift we document here has a genetic component, then the pace of evolution of

A. longimana toward their autrophic prey is rapid (i.e., less than 10 rather than 100s or

1,000s of generations) and comparable to the pace seen among terrestrial herbivorous

insects (Fry 2003), and freshwater (Hairston et al. 2001) and marine copepods (Colin

and Dam 2004). Rapid evolution has implications for studies that utilize closed-system

mesocosms and small herbivorous grazers with short generation times (e.g., A. longi-mana becomes mature within 3–4 weeks). A preliminary survey of these studies, which

include the expanding literature on grazer biodiversity and ecosystem function, reveals

a mean (±S.E.) time of duration of 5.5 ± 1.2 weeks (Range = 1–22 weeks; Table 4 in

Appendix). Given that we detected shifts (genetic or both genetic and phenotypic) in

feeding traits within time spans encompassed by some of these studies suggests pre-

vious studies in these mesocosms may partly reflect evolutionary interactions, rather

than wholly ecological phenomena as is implicitly assumed (Hairston et al. 2005). Our

results also indicate that when small short-lived herbivores are exposed to alternative

and seasonally-available hosts that generate fitness-based tradeoffs, the possibility of

fluctuating selection in host use traits across seasons should be explored (Thompson

1998).

Acknowledgments We thank Artur Veloso, John Bruno and the University of North Carolina’s Institute ofMarine Sciences for logistical support, Tina Bell, Mark Hay and Bob Podolsky for thoughtful discussions,and the National Science Foundation for funding (OCE-0550245; DEB-0919064). This is Grice PublicationNumber 364.

Appendix

See Tables 3 and 4.

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Table 3 Raw lifetable data (summarized in Fig. 3e)

1350 Evol Ecol (2011) 25:1335–1355

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Table 3 continued

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Table 4 A survey of published studies that use closed-system mesocosms and small marine herbivores

Herbivore Herbivore sp. Habitat Timespan(days)

Reference

Amphipods Mix dominated by: Hyale spp.,Elasmopus levi, Corophium spp.

Macroalgae (mix) 22 Bruno andO’Connor(2005)Isopod Paracerceis caudata

Amphipod Ampithoe longimana Macroalgae (mix) 28; 21 Bruno et al.(2008)Urchin Arbacia punctulata

Fish Lagodon rhomboides

Amphipods Gammarus mucronatus, Cymadusacompta, Ampithoe longimana

Seagrass (Zosteramarina)

42 Canuel et al.(2007)

Isopods Erichsonella attenuata, Idotea baltica

Amphipods Most abundant: Ampithoe longimanaDulichiella appendiculata

Macroalgae (mix) 154 Duffy and Hay(2000)

Isopod Paracerceis caudata

Gastropod Diastoma varium

Amphipods Gammarus mucronatus, Ampithoelongimana, Cymadusa compta


28 Duffy andHarvilicz(2001)

Amphipods Cymadusa compta, Dulichiellaappendiculata, Gammarus mucronatus


42 Duffy et al.(2003)


Amphipods Cymadusa compta, Ampithoe longimana,Gammarus mucronatus


42 Duffy et al.(2005)


Amphipods Ampithoe longimana, Cymadusa compta Seagrass (Zosteramarina)

56 France and Duffy(2006a)Isopods Erchsonella attenuata, Idotea baltica

Amphipods Gammarus mucronatus, Ampithoevalida, Cymadusa compta, Dulichiellaappendiculata, Elasmopus levis


47 France and Duffy(2006b)

Isopods Erchsonella attenuata, Idotea baltica,Paracerceis caudata

Ciliates Euplotes sp., Diophrys sp.,Eutintinnus inquilinum

Microalgae (mix) 21 Gamfeldt et al.(2005)

Gastropods Littorina littorea, L. saxatilis,L. fabalis

Periphyton 35; 56 Hillebrand et al.(2009)

Amphipod Gammarus duebenii

Isopod Idotea garnulosa

Shrimp Palaemon elegans

Isopod Idotea baltica Seagrass (Zosteramarina), epiphytes

10 Jaschinski andSommer(2008)

Amphipod Gammarus oceanicus

Gastropods Littorina littorea,Rissoa membranacea

Isopod Idotea baltica Seagrass (Zosteramarina)

7, 21 Jaschinski et al.(2009)Amphipod Gammarus salinus

Gastropod Littorina littorea

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