A Pleistocene legacy structures variation in modern seagrass ecosystems.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

Restricted Dispersal and Phenotypic Response to Water Depth in a Foundation Seagrass.

Species conservation and management benefit from precise understanding of natural patterns of dispersal and genetic variation. Using recent advances in indirect genetic methods applied to both adult plants and dispersed seeds, we find that the mean seed dispersal in a threatened marine foundation plant (the eelgrass Zostera marina) is approximately 100-200 m. This distance is surprisingly more similar to that of wind-dispersed terrestrial seeds (~10s to 100s of meters) than the passive dispersal of marine propagules via currents (~10s to 100s of kilometres). Because nearshore marine plants like Zostera are commonly distributed across strong selective gradients driven by bathymetry (depth) even within these restricted spatial scales, seeds are capable of dispersing to novel water depths and experiencing profound shifts in light availability, temperature and wave exposure. We documented strong phenotypic variation and genome-wide differentiation among plants separated by approximately the spatial scale of mean realised dispersal. This result suggests genetic isolation by environment in response to depth-related environmental gradients as one plausible explanation for this pattern. The ratio of effective to census size (or Ne/Nc) approximated 0.1%, indicating that a fraction of existing plants provides the genetic variation to allow adaptation to environmental change. Our results suggest that successful conservation of seagrass meadows that can adapt to microspatial and temporal variation in environmental conditions will be low without direct and persistent intervention using large numbers of individuals or a targeted selection of genotypes.

Co-phylogeographic structure in a disease-causing parasite and its oyster host.

With the increasing affordability of next-generation sequencing technologies, genotype-by-sequencing has become a cost-effective tool for ecologists and conservation biologists to describe a species' evolutionary history. For host­parasite interactions, genotype-by-sequencing can allow the simultaneous examination of host and parasite genomes and can yield insight into co-evolutionary processes. The eastern oyster, Crassostrea virginica, is among the most important aquacultured species in the United States. Natural and farmed oyster populations can be heavily impacted by 'dermo' disease caused by an alveolate protist, Perkinsus marinus. Here, we used restricted site-associated DNA sequencing (RADseq) to simultaneously examine spatial population genetic structure of host and parasite. We analysed 393 single-nucleotide polymorphisms (SNPs) for P. marinus and 52,100 SNPs for C. virginica from 36 individual oysters from the Gulf of Mexico (GOM) and mid-Atlantic coastline. All analyses revealed statistically significant genetic differentiation between the GOM and mid-Atlantic coast populations for both C. virginica and P. marinus, and genetic divergence between Chesapeake Bay and the outer coast of Virginia for C. virginica, but not for P. marinus. A co-phylogenetic analysis confirmed significant coupled evolutionary change between host and parasite across large spatial scales. The strong genetic divergence between marine basins raises the possibility that oysters from either basin would not be well adapted to parasite genotypes and phenotypes from the other, which would argue for caution with regard to both oyster and parasite transfers between the Atlantic and GOM regions. More broadly, our results demonstrate the potential of RADseq to describe spatial patterns of genetic divergence consistent with coupled evolution.

Phenology and thallus size in a non-native population of Gracilaria vermiculophylla.

Phenology, or seasonal variation in life cycle events, is poorly described for many macroalgal species. We describe the phenology of a non-native population of Gracilaria vermiculophylla whose thalli are free-living or anchored by decorating polychaetes to tube caps. At a site in South Carolina, USA, we sampled 100 thalli approximately every month from January 2014 to January 2015. We assessed the reproductive state and measured thallus size based on wet weight, thallus length, and thallus surface area from herbarium mounts. Because life cycle stage cannot be assigned using morphology, we implemented a PCR assay to determine the life cycle stage-tetrasporophyte, female gametophyte, or male gametophyte-of each thallus. Tetrasporophytes dominated throughout the year, making up 81%-100% of thalli sampled per month. Reproductive tetrasporophytes varied between 0% and 65% of monthly samples and were most common in warm summer months (July through September) when thalli also tended to be larger. The vast majority of the reproductive thalli were worm-anchored and not fixed to hard substratum via a holdfast. Thus, free-living thalli can be reproductive and potentially seed new non-native populations. Given G. vermiculophylla reproduction seems tied closely to temperature, our work suggests phenology may change with climate-related changes in seawater temperatures. We also highlight the importance of understanding the natural history of macroalgae to better understand the consequence of range expansions on population dynamics.

The biogeography of community assembly: latitude and predation drive variation in community trait distribution in a guild of epifaunal crustaceans.

While considerable evidence exists of biogeographic patterns in the intensity of species interactions, the influence of these patterns on variation in community structure is less clear. Studying how the distributions of traits in communities vary along global gradients can inform how variation in interactions and other factors contribute to the process of community assembly. Using a model selection approach on measures of trait dispersion in crustaceans associated with eelgrass (Zostera marina) spanning 30° of latitude in two oceans, we found that dispersion strongly increased with increasing predation and decreasing latitude. Ocean and epiphyte load appeared as secondary predictors; Pacific communities were more overdispersed while Atlantic communities were more clustered, and increasing epiphytes were associated with increased clustering. By examining how species interactions and environmental filters influence community structure across biogeographic regions, we demonstrate how both latitudinal variation in species interactions and historical contingency shape these responses. Community trait distributions have implications for ecosystem stability and functioning, and integrating large-scale observations of environmental filters, species interactions and traits can help us predict how communities may respond to environmental change.

Repeated Genetic and Adaptive Phenotypic Divergence across Tidal Elevation in a Foundation Plant Species.

AbstractMicrogeographic genetic divergence can create fine-scale trait variation. When such divergence occurs within foundation species, then it might impact community structure and ecosystem function and cause other cascading ecological effects. We tested for parallel microgeographic trait and genetic divergence in Spartina alterniflora, a foundation species that dominates salt marshes of the US Atlantic and Gulf coasts. Spartina is characterized by tall-form (1-2 m) plants at lower tidal elevations and short-form (<0.5 m) plants at higher tidal elevations, yet whether this trait variation reflects plastic and/or genetically differentiated responses to these environmental conditions remains unclear. In the greenhouse, seedlings raised from tall-form plants grew taller than those from short-form plants, indicating a heritable difference in height. When we reciprocally transplanted seedlings back into the field for a growing season, composite fitness (survivorship and seed production) and key plant traits (plant height and biomass allocation) differed interactively across origin and transplant zones in a manner indicative of local adaptation. Further, a survey of single nucleotide polymorphisms revealed repeated, independent genetic differentiation between tall- and short-form Spartina at five of six tested marshes across the native range. The observed parallel, microgeographic genetic differentiation in Spartina likely underpins marsh health and functioning and provides an underappreciated mechanism that might increase capacity of marshes to adapt to rising sea levels.

Founder effects shape linkage disequilibrium and genomic diversity of a partially clonal invader.

The genomic variation of an invasive species may be affected by complex demographic histories and evolutionary changes during the invasion. Here, we describe the relative influence of bottlenecks, clonality, and population expansion in determining genomic variability of the widespread red macroalga Agarophyton vermiculophyllum. Its introduction from mainland Japan to the estuaries of North America and Europe coincided with shifts from predominantly sexual to partially clonal reproduction and rapid adaptive evolution. A survey of 62,285 SNPs for 351 individuals from 35 populations, aligned to 24 chromosome-length scaffolds indicate that linkage disequilibrium (LD), observed heterozygosity (Ho ), Tajima's D, and nucleotide diversity (Pi) were greater among non-native than native populations. Evolutionary simulations indicate LD and Tajima's D were consistent with a severe population bottleneck. Also, the increased rate of clonal reproduction in the non-native range could not have produced the observed patterns by itself but may have magnified the bottleneck effect on LD. Elevated marker diversity in the genetic source populations could have contributed to the increased Ho and Pi observed in the non-native range. We refined the previous invasion source region to a ~50 km section of northeastern Honshu Island. Outlier detection methods failed to reveal any consistently differentiated loci shared among invaded regions, probably because of the complex A. vermiculophyllum demographic history. Our results reinforce the importance of demographic history, specifically founder effects, in driving genomic variation of invasive populations, even when localized adaptive evolution and reproductive system shifts are observed.

Intraspecific diversity and genetic structure in the widespread macroalga Agarophyton vermiculophyllum.

Single-gene markers, such as the mitochondrial cox1, microsatellites, and single-nucleotide polymorphisms are powerful methods to describe diversity within and among taxonomic groups and characterize phylogeographic patterns. Large repositories of publicly-available, molecular data can be combined to generate and evaluate evolutionary hypotheses for many species, including algae. In the case of biological invasions, the combination of different molecular markers has enabled the description of the geographic distribution of invasive lineages. Here, we review the phylogeography of the widespread invasive red macroalga Agarophyton vermiculophyllum (synonym Gracilaria vermiculophylla). The cox1 barcoding provided the first description of the invasion history and hinted at a strong genetic bottleneck during the invasion. Yet, more recent microsatellite and SNP genotyping has not found evidence for bottlenecks and instead suggested that genetically diverse inocula arose from a highly diverse source population, multiple invasions, or some mix of these processes. The bottleneck evident from cox1 barcoding likely reflects the dominance of one mitochondrial lineage, and one haplotype in particular, in the northern source populations in Japan. Recent cox1 sequencing of A. vermiculophyllum has illuminated the complexity of phylogeographic structure in its native range of the northwest Pacific Ocean. For example, the western coast of Honshu in the Sea of Japan displays spatial patterns of haplotypic diversity with multiple lineages found together at the same geographic site. By consolidating the genetic data of this species, we clarify the phylogenetic relationships of a well-studied macroalga introduced to virtually every temperate estuary of the Northern Hemisphere.

Using RAD-seq to develop sex-linked markers in a haplodiplontic alga.

For many taxa, including isomorphic haplodiplontic macroalgae, determining sex and ploidy is challenging, thereby limiting the scope of some population demographic and genetic studies. Here, we used double-digest restriction site-associated DNA sequencing (ddRAD-seq) to identify sex-linked molecular markers in the widespread red alga Agarophyton vermiculophyllum. In the ddRAD-seq library, we included 10 female gametophytes, 10 male gametophytes, and 16 tetrasporophytes from one native and one non-native site (N = 40 gametophytes and N = 32 tetrasporophytes total). We identified seven putatively female-linked and 19 putatively male-linked sequences. Four female- and eight male-linked markers amplified in all three life cycle stages. Using one female- and one male-linked marker that were sex-specific, we developed a duplex PCR and tested the efficacy of this assay on a subset of thalli sampled at two sites in the non-native range. We confirmed ploidy based on the visual observation of reproductive structures and previous microsatellite genotyping at 10 polymorphic loci. For 32 vegetative thalli, we were able to assign sex and confirm ploidy in these previously genotyped thalli. These markers will be integral to ongoing studies of A. vermiculophyllum invasion. We discuss the utility of RAD-seq over other approaches previously used, such as RAPDs (random amplified polymorphic DNA), for future work designing sex-linked markers in other haplodiplontic macroalgae for which genomes are lacking.

Plant feeding promotes diversification in the Crustacea.

About half of the world's animal species are arthropods associated with plants, and the ability to consume plant material has been proposed to be an important trait associated with the spectacular diversification of terrestrial insects. We review the phylogenetic distribution of plant feeding in the Crustacea, the other major group of arthropods that commonly consume plants, to estimate how often plant feeding has arisen and to test whether this dietary transition is associated with higher species numbers in extant clades. We present evidence that at least 31 lineages of marine, freshwater, and terrestrial crustaceans (including 64 families and 185 genera) have independently overcome the challenges of consuming plant material. These plant-feeding clades are, on average, 21-fold more speciose than their sister taxa, indicating that a shift in diet is associated with increased net rates of diversification. In contrast to herbivorous insects, most crustaceans have very broad diets, and the increased richness of taxa that include plants in their diet likely results from access to a novel resource base rather than host-associated divergence.

Mixed effects of an introduced ecosystem engineer on the foraging behavior and habitat selection of predators.

Invasive ecosystem engineers both positively and negatively affect their recipient ecosystems by generating novel habitats. Many studies have focused on alterations to ecosystem properties and to native species diversity and abundance caused by invasive engineers. However, relatively few studies have documented the extent to which behaviors of native species are affected. The red seaweed Gracilaria vermiculophylla (Rhodophyta) invaded estuaries of the southeastern United States within the last few decades and now provides abundant aboveground vegetative cover on intertidal mudflats that were historically devoid of seaweeds. We hypothesized that G. vermiculophylla would affect the foraging behavior of native shorebirds positively for birds that target seaweed-associated invertebrates or negatively for birds that target prey on or within the sediment now covered with seaweed. Visual surveys of mudflats >1 ha in size revealed that more shorebirds occurred on mudflats with G. vermiculophylla relative to mudflats without G. vermiculophylla. This increased density was consistent across 7 of 8 species, with the one exception being the semipalmated plover Charadrius semipalmatus. A regression-based analysis indicated that while algal presence predicted shorebird density, densities of some bird species depended on sediment composition and infaunal invertebrate densities. At smaller spatial scales (200 m2 and <1 m2 ), experimental removals and additions of G. vermiculophylla and focal observations showed strong variation in behavioral response to G. vermiculophylla among bird species. Birds preferentially foraged in bare mud (e.g., C. semipalmatus), in G. vermiculophylla (e.g., Arenaria interpres), or displayed no preference for either habitat (e.g., Tringa semipalmata). Thus, while the presence of the invasive ecosystem engineer on a mudflat appeared to attract greater numbers of these predators, shorebird species differed in their behavioral responses at the smaller spatial scales that affect their foraging. Our research illuminates the need to account for species identity, individual behavior, and scale when predicting the impacts of invasive species on native communities.

Latitude, temperature, and habitat complexity predict predation pressure in eelgrass beds across the Northern Hemisphere.

Latitudinal gradients in species interactions are widely cited as potential causes or consequences of global patterns of biodiversity. However, mechanistic studies documenting changes in interactions across broad geographic ranges are limited. We surveyed predation intensity on common prey (live amphipods and gastropods) in communities of eelgrass (Zostera marina) at 48 sites across its Northern Hemisphere range, encompassing over 37° of latitude and four continental coastlines. Predation on amphipods declined with latitude on all coasts but declined more strongly along western ocean margins where temperature gradients are steeper. Whereas in situ water temperature at the time of the experiments was uncorrelated with predation, mean annual temperature strongly positively predicted predation, suggesting a more complex mechanism than simply increased metabolic activity at the time of predation. This large-scale biogeographic pattern was modified by local habitat characteristics; predation declined with higher shoot density both among and within sites. Predation rates on gastropods, by contrast, were uniformly low and varied little among sites. The high replication and geographic extent of our study not only provides additional evidence to support biogeographic variation in predation intensity, but also insight into the mechanisms that relate temperature and biogeographic gradients in species interactions.

Nonnative Gracilaria vermiculophylla tetrasporophytes are more difficult to debranch and are less nutritious than gametophytes.

Theory predicts that the maintenance of haplodiplontic life cycles requires ecological differences between the haploid gametophytes and diploid sporophytes, yet evidence of such differences remain scarce. The haplodiplontic red seaweed Gracilaria vermiculophylla has invaded the temperate estuaries of the Northern Hemisphere, where it commonly modifies detrital and trophic pathways. In native populations, abundant hard substratum enables spore settlement, and gametophyte:tetrasporophyte ratios are ~40:60. In contrast, many non-native populations persist in soft-sediment habitats without abundant hard substratum, and can be 90%-100% tetrasporophytic. To test for ecologically relevant phenotypic differences, we measured thallus morphology, protein content, organic content, "debranching resistance" (i.e., tensile force required to remove a branch from its main axis node), and material properties between male gametophytes, female gametophytes, and tetrasporophytes from a single, nonnative site in Charleston Harbor, South Carolina, USA in 2015 and 2016. Thallus length and surface area to volume ratio differed between years, but were not significantly different between ploidies. Tetrasporophytes had lower protein content than gametophytes, suggesting the latter may be more attractive to consumers. More force was required to pull a branch from the main axis of tetrasporophytes relative to gametophytes. A difference in debranching resistance may help to maintain tetrasporophyte thallus durability relative to gametophytes, providing a potential advantage in free-floating populations. These data may shed light on the invasion ecology of an important ecosystem engineer, and may advance our understanding of life cycle evolution and the maintenance of life cycle diversity.

Declines in plant palatability from polar to tropical latitudes depend on herbivore and plant identity.

Long-standing theory predicts that the intensity of consumer-prey interactions declines with increasing latitude, yet for plant-herbivore interactions, latitudinal changes in herbivory rates and plant palatability have received variable support. The topic is of growing interest given that lower-latitude species are moving poleward at an accelerating rate due to climate change, and predicting local interactions will depend partly on whether latitudinal gradients occur in these critical biotic interactions. Here, we assayed the palatability of 50 seaweeds collected from polar (Antarctica), temperate (northeastern Pacific; California), and tropical (central Pacific; Fiji) locations to two herbivores native to the tropical and subtropical Atlantic, the generalist crab Mithraculus sculptus and sea urchin Echinometra lucunter. Red seaweeds (Rhodophyta) of polar and temperate origin were more readily consumed by urchins than were tropical reds. The decline in palatability with decreasing latitude is explained by shifts in tissue organic content along with the quantity and quality of secondary metabolites, degree of calcification or both. We detected no latitudinal shift in palatability of red seaweeds to crabs, nor any latitudinal shifts in palatability of brown seaweeds (Phaeophyta) to either crabs or urchins. Our results suggest that evolutionary pressure from tropical herbivores favored red seaweeds with lower palatability, either through the production of greater levels of chemical defenses, calcification, or both. Moreover, our results tentatively suggest that the "tropicalization" of temperate habitats is facilitated by the migration of tropical herbivores into temperate areas dominated by weakly defended and more nutritious foods, and that the removal of these competing seaweeds may facilitate the invasion of better-defended tropical seaweeds.

Invasion of novel habitats uncouples haplo-diplontic life cycles.

Baker's Law predicts uniparental reproduction will facilitate colonization success in novel habitats. While evidence supports this prediction among colonizing plants and animals, few studies have investigated shifts in reproductive mode in haplo-diplontic species in which both prolonged haploid and diploid stages separate meiosis and fertilization in time and space. Due to this separation, asexual reproduction can yield the dominance of one of the ploidy stages in colonizing populations. We tested for shifts in ploidy and reproductive mode across native and introduced populations of the red seaweed Gracilaria vermiculophylla. Native populations in the northwest Pacific Ocean were nearly always attached by holdfasts to hard substrata and, as is characteristic of the genus, haploid-diploid ratios were slightly diploid-biased. In contrast, along North American and European coastlines, introduced populations nearly always floated atop soft-sediment mudflats and were overwhelmingly dominated by diploid thalli without holdfasts. Introduced populations exhibited population genetic signals consistent with extensive vegetative fragmentation, while native populations did not. Thus, the ecological shift from attached to unattached thalli, ostensibly necessitated by the invasion of soft-sediment habitats, correlated with shifts from sexual to asexual reproduction and slight to strong diploid bias. We extend Baker's Law by predicting other colonizing haplo-diplontic species will show similar increases in asexuality that correlate with the dominance of one ploidy stage. Labile mating systems likely facilitate colonization success and subsequent range expansion, but for haplo-diplontic species, the long-term eco-evolutionary impacts will depend on which ploidy stage is lost and the degree to which asexual reproduction is canalized.

Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach.

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

The Adaptive Cline at LDH (Lactate Dehydrogenase) in Killifish Fundulus heteroclitus Remains Stationary After 40 Years of Warming Estuaries.

Since the 1970s, water temperatures along the Atlantic seaboard of the United States have risen by an average of 0.5 °C in summer months and 2.2 °C in winter months. In response, the distribution and abundance of several nearshore species have changed dramatically, but no study has attempted to document whether estuarine populations have evolved greater thermal tolerance. Here, we re-examine the classic latitudinal cline at lactate dehydrogenase (LDH) in the killifish Fundulus heteroclitus that was originally described by Dennis Powers and associates from samples collected between 1970 and 1972. Laboratory and field evidences indicated that northern and southern isozymes at muscle LDH are locally adapted to cold and warm temperatures, respectively. Despite the potential for evolutionary response at this adaptive locus, we detected no significant shift of the LDH cline from 20 to 30 F. heteroclitus collected at each of 13 locations between the early 1970s and 2010. We conclude that the microevolution of LDH-mediated thermal tolerance has not occurred, that shifts in alleles are too incremental to be distinguished from random processes, or that F. heteroclitus uses phenotypic and genetic mechanisms besides LDH to respond to warmer waters.

The relative importance of predation risk and water temperature in maintaining Bergmann's rule in a marine ectotherm.

Bergmann's rule-an increase in body size with latitude-correlates with latitudinal declines in ambient temperature and predation risk, but relatively few studies simultaneously explore the relative importance of these factors. Along temperate Atlantic shorelines, the isopod Idotea balthica from high latitudes are 53% longer on average than isopods from low latitudes. When reared at 6°-24°C, juveniles increased growth and development rates with temperature. Because the increase in growth rate with temperature outstripped increases in development rate, female size at maturity increased with temperature. This thermal sensitivity of growth cannot account for the latitudinal pattern in body size. Within temperature treatments, females from low latitudes reached sexual maturity at younger ages and at a smaller size than did females from higher latitudes. This shift in life-history strategy is predicted by latitudinal declines in predation pressure, which we tested using field-tethering experiments. Overall, isopods at low latitudes had a 44% greater mortality risk from daytime predators relative to isopods at higher latitudes. We conclude that a latitudinal gradient in predation risk, not temperature, is principally responsible for Bergmann's rule in I. balthica. Increases in body size during future warming of oceans may be constrained by local patterns of predation risk.

Biogeographic and phylogenetic effects on feeding resistance of generalist herbivores toward plant chemical defenses.

Many terrestrial and most marine herbivores have generalist diets, yet the role that evolutionary history plays in their foraging behaviors is poorly documented. On tropical hard-bottom reefs, generalist fishes and sea urchins readily consume seaweeds that produce lipophilic secondary metabolites. In contrast, herbivores on temperate reefs less commonly encounter seaweeds with analogous metabolites. This biogeographic pattern suggests that tropical herbivores should evolve greater feeding resistance to lipophilic defenses relative to temperate herbivores, but tests of this biogeographic pattern are rare. We offered lipophilic extracts from nine subtropical seaweeds at two concentrations to sea urchins (four subtropical and three cold-temperate populations) and quantified urchin feeding resistance. Patterns of feeding resistance toward lipophilic defenses were more similar within genera than across genera of urchins, indicating a substantial role for phylogenetic history in the feeding ecology of these generalist herbivores. The biogeographic origin of urchins also influenced feeding resistance, as subtropical species displayed greater feeding resistance than did temperate species. Similarly, a subtropical population of Arbacia punctulata had greater feeding resistance for Dictyota and Stypopodium extracts relative to temperate A. punctulata. We conclude that evolutionary history plays a more central role in the foraging ecology of generalist herbivores than is currently appreciated.

Geographic variation in feeding preference of a generalist herbivore: the importance of seaweed chemical defenses.

The ecological impacts of generalist herbivores depend on feeding preferences, which can vary across and within herbivore species. Among mesoherbivores, geographic variation in host use can occur because host plants have a more restricted geographic distribution than does the herbivore, or there is local evolution in host preference, or both. We tested the role of local evolution using the marine amphipod Ampithoe longimana by rearing multiple amphipod populations from three regions (subtropical Florida, warm-temperate North Carolina and cold-temperate New England) and assaying their feeding preferences toward ten seaweeds that occur in some but not all regions. Six of the ten seaweeds produce anti-herbivore secondary metabolites, and we detected geographic variation in feeding preference toward five (Dictyota menstrualis, Dictyota ciliolata, Fucus distichus, Chondrus crispus and Padina gymnospora, but not Caulerpa sertularioides). Amphipod populations that co-occur with a chemically-rich seaweed tended to have stronger feeding preferences for that seaweed, relative to populations that do not co-occur with the seaweed. A direct test indicated that geographic variation in feeding preference toward one seaweed (D. ciliolata) is mediated by feeding tolerance for lipophilic secondary metabolites. Among the four seaweeds that produce no known secondary metabolites (Acanthophora, Ectocarpus, Gracilaria and Hincksia/Feldmannia spp.), we detected no geographic variation in feeding preference. Thus, populations are more likely to evolve greater feeding preferences for local hosts when those hosts produce secondary metabolites. Microevolution of feeding behaviors of generalist marine consumers likely depends on the availability and identity of local hosts and the strength of their chemical defenses.