Algal Genotypes Research Articles

From the shallow to the mesophotic: a characterization of Symbiodiniaceae diversity in the Red Sea NEOM region

IntroductionThe northern Red Sea has been coined a refuge for reef corals due to the exceptional thermal tolerance of these organisms. With ocean warming threatening coral reefs worldwide, a panoptic characterization of corals living in extreme conditions may provide insights into future responses of corals to environmental change. Among other factors, the genotype of the endosymbiotic algae in the family Symbiodiniaceae has been shown to have major implications on the distribution and resilience of their coral hosts. In this study, we aim at genotyping the Symbiodiniaceae communities associated with three depth generalist and one depth specialist coral species, characterized by the ability to withstand environmental conditions that are apparently limiting for other corals and occurring in a unique geographical region.MethodsWe sampled 50 corals from the northern Saudi Arabian Red Sea and the Gulf of Aqaba, covering a 97 m bathymetric gradient. We used high-throughput ITS2 gene sequencing and recovered different patterns of host–algal associations.Results and discussionThe majority of the recovered algal genotypes appeared host- and environment-specific, while others were more widely distributed. At large, coral specimens were overwhelmingly associated with symbionts from the genus Cladocopium and specifically with many previously undescribed genotypes. This suggests the selection of specific genotypes, which might confer resistance and/or resilience to their host counterparts. Interestingly, we found a limited association with Durusdinium spp. and other known tolerant taxa in mesophotic corals in the northern Red Sea, but not in the Gulf of Aqaba. The broad absence of Durusdinium spp., typically ascribed to be stress tolerant, warrants further investigation into Symbiodiniaceae species that convey environmental resilience. Our data will serve as a baseline to explore the occurrence of specific symbionts that might be contributing to coral acclimation and adaptation and to assay how biodiversity might be impacted if subjected to increasing stressors.

Climate warming causes photobiont degradation and carbon starvation in a boreal climate sentinel lichen.

The long-term potential for acclimation by lichens to changing climates is poorly known, despite their prominent roles in forested ecosystems. Although often considered "extremophiles," lichens may not readily acclimate to novel climates well beyond historical norms. In a previous study (Smith et al., 2018), Evernia mesomorpha transplants in a whole-ecosystem climate change experiment showed drastic mass loss after 1 yr of warming and drying; however, the causes of this mass loss were not addressed. We examined the causes of this warming-induced mass loss by measuring physiological, functional, and reproductive attributes of lichen transplants. Severe loss of mass and physiological function occurred above +2°C of experimental warming. Loss of algal symbionts ("bleaching") and turnover in algal community compositions increased with temperature and were the clearest impacts of experimental warming. Enhanced CO2 had no significant physiological or symbiont composition effects. The functional loss of algal photobionts led to significant loss of mass and specific thallus mass (STM), which in turn reduced water-holding capacity (WHC). Although algal genotypes remained detectable in thalli exposed to higher stress, within-thallus photobiont communities shifted in composition toward greater diversity. The strong negative impacts of warming and/or lower humidity on Evernia mesomorpha were driven by a loss of photobiont activity. Analogous to the effects of climate change on corals, the balance of symbiont carbon metabolism in lichens is central to their resilience to changing conditions.

Fungal Host Affects Photosynthesis in a Lichen Holobiont.

Corals and lichens are iconic examples of photosynthetic holobionts, i.e., ecological and evolutionary units resulting from the tightly integrated association of algae and prokaryotic microbiota with animal or fungal hosts, respectively. While the role of the coral host in modulating photosynthesis has been clarified to a large extent in coral holobionts, the role of the fungal host in this regard is far less understood. Here, we address this question by taking advantage of the recent discovery of highly specific fungal-algal pairings corresponding to climatically adapted ecotypes of the lichen-forming genus Umbilicaria. Specifically, we compared chlorophyll a fluorescence kinetics among lichen thalli consisting of different fungal-algal combinations. We show that photosynthetic performance in these lichens is not only driven by algal genotype, but also by fungal host species identity and intra-host genotype. These findings shed new light on the closely intertwined physiological processes of fungal and algal partners in the lichen symbiosis. Indeed, the specific combinations of fungal and algal genotypes within a lichen individual-and the resulting combined functional phenotype-can be regarded as a response to the environment. Our findings suggest that characterizing the genetic composition of both eukaryotic partners is an important complimentary step to understand and predict the lichen holobiont's responses to environmental change.

Symbiont genotype influences holobiont response to increased temperature

As coral reefs face warming oceans and increased coral bleaching, a whitening of the coral due to loss of microalgal endosymbionts, the possibility of evolutionary rescue offers some hope for reef persistence. In tightly linked mutualisms, evolutionary rescue may occur through evolution of the host and/or endosymbionts. Many obligate mutualisms are composed of relatively small, fast-growing symbionts with greater potential to evolve on ecologically relevant time scales than their relatively large, slower growing hosts. Numerous jellyfish species harbor closely related endosymbiont taxa to other cnidarian species such as coral, and are commonly used as a model system for investigating cnidarian mutualisms. We examined the potential for adaptation of the upside-down jellyfish Cassiopea xamachana to increased temperature via evolution of its microalgal endosymbiont, Symbiodinium microadriaticum. We quantified trait variation among five algal genotypes in response to three temperatures (26 °C, 30 °C, and 32 °C) and fitness of hosts infected with each genotype. All genotypes showed positive growth rates at each temperature, but rates of respiration and photosynthesis decreased with increased temperature. Responses varied among genotypes but were unrelated to genetic similarity. The effect of temperature on asexual reproduction and the timing of development in the host also depended on the genotype of the symbiont. Natural selection could favor different algal genotypes at different temperatures, affecting host fitness. This eco-evolutionary interaction may be a critical component of understanding species resilience in increasingly stressful environments.

Short communication: Algal genotypes in White Syndrome infected coral Acropora muricata from the Karimunjawa Islands, Indonesia

Abstract. Wijayanti DP, Nadia M, Indrayanti E, Haryanti D, Bachtiar M. 2021. Short communication: Algal genotypes in White Syndrome infected coral Acropora muricata from the Karimunjawa Islands, Indonesia. Biodiversitas 23: 415-423. The physiological equilibrium of the coral holobiont may help the corals to survive under various environmental threats. The symbiont genotype is thought to play an important role in the host's susceptibility to thermal stress and coral disease incidence. We identified the Symbiodiniaceae diversity of coral Acropora muricata infected by White Syndrome (WS). Samples were collected from Cemara Kecil Island and Barakuda Beach, Kemujan Island, Karimunjawa Islands. We applied DNA barcoding of 28S nuclear ribosomal RNA gene of the healthy colonies, healthy tissue, and lesions of diseased colonies to perform their symbiont type identification. There were two different symbiont types observed from the phylogenetic analysis, which formed two clades. A clade consisting all Cemara Kecil Island samples while the other with all Barakuda Beach samples except for one. All samples harbored symbiont types from the genus Cladocopium. The members of the genus were reported to have various physiological properties which may support the host resilience when facing the disease. A robust study is needed to reveal the influence of symbiont genotypes on the occurrence of coral disease and the susceptibility of the coral host.

Flexibility in Red Sea Tridacna maxima-Symbiodiniaceae associations supports environmental niche adaptation.

Giant clams (Tridacninae) are important members of Indo‐Pacific coral reefs and among the few bivalve groups that live in symbiosis with unicellular algae (Symbiodiniaceae). Despite the importance of these endosymbiotic dinoflagellates for clam ecology, the diversity and specificity of these associations remain relatively poorly studied, especially in the Red Sea. Here, we used the internal transcribed spacer 2 (ITS2) rDNA gene region to investigate Symbiodiniaceae communities associated with Red Sea Tridacna maxima clams. We sampled five sites spanning 1,300 km (10° of latitude, from the Gulf of Aqaba, 29°N, to the Farasan Banks, 18°N) along the Red Sea's North‐South environmental gradient. We detected a diverse and structured assembly of host‐associated algae with communities demonstrating region and site‐specificity. Specimens from the Gulf of Aqaba harbored three genera of Symbiodiniaceae, Cladocopium, Durusdinium, and Symbiodinium, while at all other sites clams associated exclusively with algae from the Symbiodinium genus. Of these exclusively Symbiodinium‐associating sites, the more northern (27° and 22°) and more southern sites (20° and 18°) formed two separate groupings despite site‐specific algal genotypes being resolved at each site. These groupings were congruent with the genetic break seen across multiple marine taxa in the Red Sea at approximately 19°, and along with our documented site‐specificity of algal communities, contrasted the panmictic distribution of the T. maxima host. As such, our findings indicate flexibility in T. maxima‐Symbiodiniaceae associations that may explain its relatively high environmental plasticity and offers a mechanism for environmental niche adaptation.

Lichen-forming fungi in postindustrial habitats involve alternative photobionts

ABSTRACT Mycobionts of many lichen genera appear to demonstrate strong selectivity in the choice of algal partner. The biological properties of a photobiont and its availability in an environment significantly determine the habitat requirements of lichens. Flexibility in photobiont choice extends the ecological amplitude of lichens; therefore, it may constitute an important adaptive strategy for colonization of extreme habitats. The photobiont inventory of the three epigeic lichens most resistant to soil pollution, i.e., Cladonia cariosa, C. rei, and the hyperaccumulator Diploschistes muscorum, was examined to verify whether and to what extent algal composition depends on the type of habitat and substrate enrichment with heavy metals. Photobionts Asterochloris and Trebouxia were identified in the studied lichen species; however, the presence of Trebouxia was directly related to anthropogenic sites with technogenic substrates, and the proportion of lichen specimens with these algae clearly depended on the level of heavy-metal soil pollution and the habitat type. The total number of algal haplotypes increased with increasing soil pollution, and the richness was associated more with soil pollution than with a given lichen species. Additionally, a large number of lichen individuals bearing multiple algal genotypes at polluted sites were recorded. Although Cladonia lichens were previously thought to be restricted to Asterochloris, they are able to start the relichenization process with Trebouxia under specific habitat conditions and to establish a stable association with these algae when colonization of disturbed sites takes place. Comparative analysis of the internal transcribed spacer (ITS) rDNA sequences revealed as many as 13 haplotypes of Trebouxia, and phylogenetic analysis grouped them into two different clades. Such a high level of genetic diversity indicates that Trebouxia is well adapted to metal pollution and could be an alternative photosynthetic partner for certain lichens, especially in polluted sites.

Heavy-metal pollution induces changes in the genetic composition and anatomical properties of photobionts in pioneer lichens colonising post-industrial habitats

Certain lichens are effective colonisers of polluted sites. However, little is known about the tolerance of photobionts and the degree of mycobiont selectivity to photobionts relative to metal pollution. The present study recognises the genetic and anatomical diversity of Asterochloris photobionts in epigeic lichens, i.e. Cladonia cariosa, C. rei, and Diploschistes muscorum, in relation to a wide spectrum of soil pollution. In accordance with phylogenetic analysis, photobionts were clustered in 7 moderately- to well-supported clades, including 19 haplotypes. The mycobionts of all studied lichens demonstrated a low level of selectivity and were capable of associating with various Asterochloris lineages. This tendency was also expressed by the frequent (~25%) occurrence of multiple algal genotypes in a single thallus. This indicates that identified Asterochloris lineages are generally tolerant to heavy-metal pollution, and the low level of selectivity of mycobionts enables them to select the most suitable and/or available partner. The trend of increasing incidence of certain Asterochloris lineages and decreasing frequency of others along with increasing soil pollution was observed. This proves the superior adaptation of some photobionts to polluted sites. Such symbiotic plasticity constitute an adaptive feature necessary for the successful colonisation. High number of haplotypes at polluted sites could be the result of multiple introduction events from different areas during the initial stages of spontaneous succession. Regardless of the genetic pattern, Asterochloris cells were considerably smaller, and the density and compaction of cells in the algal layer were higher, in lichen specimens from polluted sites, indicating that photobiont characteristics may be closely dependent on heavy-metal pollution.

Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations

Widespread coral bleaching occurred in the central Red Sea in 2010 and 2015. During both events, a cross-shelf and depth gradient of bleaching severity was identified within the Thuwal reef system, central Red Sea, Saudi Arabia. While bleaching and survival of coral taxa were monitored, neither in situ reef temperatures nor coral-associated algal communities (family Symbiodiniaceae) were characterized. Here, we determined coral host-associated Symbiodiniaceae communities and monitored temperatures along the same cross-shelf and depth gradient on six reefs in 2017 to better understand the role of these factors in the observed bleaching patterns and to generate a baseline for further studies. We characterized > 600 coral–algal associations across winter and summer in six genera of scleractinian coral (Pocillopora, Stylophora, Seriatopora, Galaxea, Gardineroseris, and Porites) and one fire coral (Family Milleporidae) using ITS2 next-generation sequencing in conjunction with the SymPortal analytical framework. We show that previous bleaching patterns correlate poorly with the largely coral host-specific structure of the 2017 Symbiodiniaceae community and are in better agreement with absolute and intraday sea water temperature variations monitored on the reefs. We demonstrate a greater distinctiveness of Symbiodiniaceae communities at the more severely bleached inshore reefs compared to those reefs further offshore. However, the potential Symbiodiniaceae community changes at these reefs prior to our sampling prevent us from evaluating this distinctiveness as determinative of the differences in bleaching severities. Based on our analyses, we discuss how fine-scale delineation of algal genotypes, including host-specific putative genotypes of Durusdinium trenchii that represent alluring targets for further taxonomic identification, corroborate a niche-adapted rather than generalist character of many coral–Symbiodiniaceae associations. In conclusion, as studies such as this one continue to build the global catalogue of coral–Symbiodiniaceae associations, we may be afforded a better oversight of how specialized coral–algal associations really are and how restricted their modification may be, both of which are critical considerations in predicting the adaptive potential of corals and the reef ecosystems they build.

Water‐borne defence induction of a rockweed in the wild

Abstract Laboratory‐scale studies suggest that water‐borne chemical cues released in grazing of marine macroalgae act as info‐chemicals allowing the yet‐undamaged conspecifics to increase their resistance before the actual herbivore attack. The relevance of this finding in natural populations has thus far remained unexplored. We investigated spread of water‐borne herbivore resistance in a field experiment using the littoral foundation species Fucus vesiculosus. We exposed algal genotypes for water‐borne cues in the distances of 0.5 and 2 m from the grazed cue‐emitting genotypes. We measured herbivore resistance with preference experiments and recorded changes in the phlorotannin content. We recorded changes in biomass and length of the genotypes to test whether water‐borne resistance correlates with the grazing damage on the cue‐emitter or incurs costs for the genotypes in terms of reduced growth. In two of our four experimental blocks, induced resistance via water‐borne cues took place and spread to undamaged neighbours that were 2 m distance apart. This provides evidence of water‐borne resistance induction in the wild as well as of small‐scale spatial variation in the spread of induction. The undamaged neighbours induced resistance to a lesser extent than the directly grazed cue‐emitters did, but resistance was consistently expressed among all 26 algal genotypes and independent of the amount of grazing damage on the cue‐emitter. Herbivore resistance correlated negatively with the growth in the grazed cue‐emitting genotypes, while water‐borne resistance was independent of the variation in growth. Our results show, for the first time for marine macroalgae in a natural setting, that information about the increased risk of herbivory can be carried by water‐borne cues and is used to prime or induce defences prior to an actual attack. The results we present furthermore indicate that water‐borne resistance differs quantitatively and qualitatively from the resistance triggered by actively feeding herbivores. Ability to induce resistance prior the herbivore arrival may greatly influence the ability of littoral macroalgae to withstand the generally intense herbivory of marine benthic environments. A plain language summary is available for this article.

Algal and fungal diversity in Antarctic lichens.

The composition of lichen ecosystems except mycobiont and photobiont has not been evaluated intensively. In addition, recent studies to identify algal genotypes have raised questions about the specific relationship between mycobiont and photobiont. In the current study, we analyzed algal and fungal community structures in lichen species from King George Island, Antarctica, by pyrosequencing of eukaryotic large subunit (LSU) and algal internal transcribed spacer (ITS) domains of the nuclear rRNA gene. The sequencing results of LSU and ITS regions indicated that each lichen thallus contained diverse algal species. The major algal operational taxonomic unit (OTU) defined at a 99% similarity cutoff of LSU sequences accounted for 78.7-100% of the total algal community in each sample. In several cases, the major OTUs defined by LSU sequences were represented by two closely related OTUs defined by 98% sequence similarity of ITS domain. The results of LSU sequences indicated that lichen-associated fungi belonged to the Arthoniomycetes, Eurotiomycetes, Lecanoromycetes, Leotiomycetes, and Sordariomycetes of the Ascomycota, and Tremellomycetes and Cystobasidiomycetes of the Basidiomycota. The composition of major photobiont species and lichen-associated fungal community were mostly related to the mycobiont species. The contribution of growth forms or substrates on composition of photobiont and lichen-associated fungi was not evident.

Green-algal photobiont diversity (Trebouxia spp.) in representatives of Teloschistaceae (Lecanoromycetes, lichen-forming ascomycetes)

AbstractThe green algal photobionts of 12 Xanthoria, seven Xanthomendoza, two Teloschistes species and Josefpoeltia parva (all Teloschistaceae) were analyzed. Xanthoria parietina was sampled on four continents. More than 300 photobiont isolates were brought into sterile culture. The nuclear ribosomal internal transcribed spacer region (nrITS; 101 sequences) and the large subunit of the RuBiSco gene (rbcL; 54 sequences) of either whole lichen DNA or photobiont isolates were phylogenetically analyzed. ITS and rbcL phylogenies were congruent, although some subclades had low bootstrap support. Trebouxia arboricola,T. decolorans and closely related, unnamed Trebouxia species, all belonging to clade A, were found as photobionts of Xanthoria species. Xanthomendoza species associated with either T. decolorans (clade A), T. impressa, T. gelatinosa (clade I) or with an unnamed Trebouxia species. Trebouxia gelatinosa genotypes (clade I) were the photobionts of Teloschistes chrysophthalmus,T. hosseusianus and Josefpoeltia parva. Only weak correlations between distribution patterns of algal genotypes and environmental conditions or geographical location were observed.

Effect of temperature on two reef-building corals Pocillopora damicornis and P. verrucosa in the Red Sea

The effects of temperature on two reef building corals Pocillopora damicornis and P. verrucosa inhabiting the Obhur Creek, a small embayment on the western, Red Sea coast of Saudi Arabia, was studied from December 2009 to November 2010. The overall annual range of seawater temperature in Obhur Creek was between 24.5°C and 33°C. Zooxanthellae abundance and diversity showed seasonal variations: the number of zooxanthellae in P. damicornis was slightly higher than in P. verrucosa, and the abundance of zooxanthellae of both species was low in summer and high during winter. The respiration rate of P. verrucosa did not vary between summer and winter, suggesting compensatory acclimation. In contrast, the respiratory rate in P. damicornis was lower in winter than in summer. During the winter season the metabolic rate was higher in both species owing to the optimum seawater temperature (30°C). As a result of the abundance of zooxanthellae and the optimum seawater temperature, the growth rates of the skeletons of the two coral species were higher in winter and lower in summer. In general, the results showed that P. verrucosa is more flexible with respect to temperature than P. damicornis. The difference in zooxanthellae thermal tolerances at 35°C may be due to the algal genotypes between the two species, resulting in P. damicornis becoming bleached as the rate of metabolism exceeds the rate of photosynthesis with increasing temperature.

Congruent Genetic Structure in the Lichen-Forming Fungus Lobaria pulmonaria and Its Green-Algal Photobiont

The extent of codispersal of symbionts is one of the key factors shaping genetic structures of symbiotic organisms. Concordant patterns of genetic structure are expected in vertically transmitted symbioses, whereas horizontal transmission generally uncouples genetic structures unless the partners are coadapted. Here, we compared the genetic structures of mutualists, the lichen-forming fungus Lobaria pulmonaria and its primary green-algal photobiont, Dictyochloropsis reticulata. We performed analysis of molecular variance and variogram analysis to compare genetic structures between symbiosis partners. We simulated the expected number of multilocus-genotype recurrences to reveal whether the distribution of multilocus genotypes of either species was concordant with panmixia. Simulations and tests of linkage disequilibrium provided compelling evidence for the codispersal of mutualists. To test whether genotype associations between symbionts were consistent with randomness, as expected under horizontal transmission, we simulated the recurrence of fungal-algal multilocus genotype associations expected by chance. Our data showed nonrandom associations of fungal and algal genotypes. Either vertical transmission or horizontal transmission coupled with coadaptation between symbiont genotypes may have created these nonrandom associations. This study is among the first to show codispersal and highly congruent genetic structures in the partners of a lichen mutualism.

Photobiont diversity in lichens from metal-rich substrata based on ITS rDNA sequences

The photobiont is considered as the more sensitive partner of lichen symbiosis in metal pollution. For this reason the presence of a metal tolerant photobiont in lichens may be a key factor of ecological success of lichens growing on metal polluted substrata. The photobiont inventory was examined for terricolous lichen community growing in Cu mine-spoil heaps derived by historical mining. Sequences of internal transcribed spacer (ITS) were phylogenetically analyzed using maximum likelihood analyses. A total of 50 ITS algal sequences were obtained from 22 selected lichen taxa collected at three Cu mine-spoil heaps and two control localities. Algae associated with Cladonia and Stereocaulon were identified as members of several Asterochloris lineages, photobionts of cetrarioid lichens clustered with Trebouxia hypogymniae ined. We did not find close relationship between heavy metal content (in localities as well as lichen thalli) and photobiont diversity. Presence of multiple algal genotypes in single lichen thallus has been confirmed.

Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore.

In the marine littoral, strong grazing pressure selects for macroalgal defenses such as the constitutive and inductive production of defense metabolites. Induced defenses are expected under spatiotemporally varying grazing pressure and should be triggered by a reliable cue from herbivory, thereby reducing grazing pressure via decreased herbivore preference and/or performance. Although induced resistance has frequently been demonstrated in brown macroalgae, it is yet to be investigated whether induced macroalgal resistance shows genetic variation, a prerequisite for evolutionary responses to selection. In addition, consequences of induced resistance on herbivore performance have rarely been tested while the role of brown algal phlorotannins as inducible defense metabolites remains ambiguous. Using preference bioassays, we tested various cues, e.g., natural grazing, waterborne cues or simulated grazing to induce resistance in the brown alga Fucus vesiculosus. Further, we investigated whether there are induced responses in phlorotannin content, genetic variation in induced resistance or incurred performance costs to the mesoherbivore isopod, Idotea baltica. We found that both direct grazing and waterborne grazing cues decreased the palatability of F. vesiculosus, while increasing the total phlorotannin content. Since the sole presence of the herbivore also increased the total soluble phlorotannins, yet failed to stimulate deterrence, we concluded that phlorotannins alone do not explain increased resistance. Induced resistance varied between algal genotypes and thus showed potential for evolutionary responses to variation in grazing pressure. Induced resistance also incurred performance costs for female I. baltica via reduced egg production. Our results show that the induced resistance of F. vesiculosus decreases grazing pressure by deterring herbivores as well as impairing their performance. Resistance may be induced in advance by waterborne cues and spread effectively throughout the F. vesiculosus belt. Through lowering herbivore performance, induced resistance may also reduce future grazing pressure by decreasing the population growth rate of I. baltica.

Genetically divergent algae shape an epiphytic lichen community on Jack Pine in Manitoba

AbstractAlgal genotypes should freely associate with different lichen fungi that grow in the same confined habitat giving the appearance of low levels of selectivity and specificity. If genetic compatibility between algal and fungal partners limits the combination of partners, then some degree of taxonomic specificity should be evident. This study examined the photobiont composition in a community of epiphytic lichens on Jack Pine to investigate selectivity and specificity. The objectives of the study were to infer algal identity, to infer photobiont dispersal, and to investigate the distribution of algal genotypes relative to the fungal partner. Photobiont variability was determined by Restriction Fragment Length Polymorphism (RFLP) and nucleotide sequences of the Internal Transcribed Spacer (ITS) of ribosomal DNA (rDNA). Seven species of lichen-forming fungi are reported to associate with five divergent algal genotypes, with only one species,Evernia mesomorpha, showing some degree of selectivity and specificity. The algae represent at least two species (Trebouxia jamesiiandT. impressa) for the area confined to 200cm2on the north side of 20 Jack Pine trees. Gene flow was inferred in this tightly defined community of lichenized algae. The algal sharing and inferred gene flow may suggest that soredia provide a means of algal transport and distribution among lichen-forming fungi in the habitat.

Fouling mediates grazing: intertwining of resistances to multiple enemies in the brown alga Fucus vesiculosus.

Macroalgae have to cope with multiple natural enemies, such as herbivores and epibionts. As these are harmful for the host, the host is expected to show resistance to them. Evolution of resistance is complicated by the interactions among the enemies and the genetic correlations among resistances to different enemies. Here, we explored genetic variation in resistance to epibiosis and herbivory in the brown alga Fucus vesiculosus, both under conditions where the enemies coexisted and where they were isolated. F. vesiculosus showed substantial genetic variation in the resistance to both epibiosis and grazing. Grazing pressure on the alga was generally lower in the presence than in the absence of epibiota. Furthermore, epibiosis modified the susceptibility of different algal genotypes to grazing. Resistances to epibiosis and grazing were independent when measured separately for both enemies but positively correlated when both these enemies coexisted. Thus, when the enemies coexisted, the fate of genotypes with respect to these enemies was intertwined. Genotypic correlation between phlorotannins, brown-algal phenolic secondary metabolites, and the amount of epibiota was negative, indicating that these compounds contribute to resistance to epibiosis. In addition, phlorotannins correlated also with the resistance to grazing, but this correlation disappeared when grazing occurred in the absence of epibiota. This indicates that the patterns of selection for the type of the resistance as well as for the resistance traits vary with the occurrence patterns of the enemies.

In “Cryptic” Population Dynamics, Absence of Evidence Is Not Evidence of Absence

When the populations of two species oscillate together, it’s a good bet that they are tightly coupled ecologically. Most often, these oscillations occur between predator and prey (or a pathogen and its host), as demonstrated by the famous case of the Canadian lynx and snowshoe hare, documented in the trapping records of the Hudson’s Bay Company. This makes sense—as the predator depletes the prey, its own reproduction suffers and its numbers decline; as predation eases, the prey’s numbers can grow again. But is the opposite also true? If the prey’s population doesn’t fluctuate while the predator’s does, may we assume they are not tightly linked in the food web? Among ecologists, this has generally been thought to be the case. But a new study by Takehito Yoshida and colleagues shows that this assumption is not always justified. The authors noticed some odd population dynamics in studying a rotifer and its food source, a unicellular alga. They observed the pair in a chemostat, an aqueous growth chamber whose nutrient supply is kept steady through a continuous in- and outflow of medium. Observations of the two species have shown that indeed they are tightly linked—the algae are the only food source for the rotifers—and under many conditions within this system, their populations co-oscillate like the lynx and hare. But the authors found that under other conditions, the rotifer’s population waxed and waned, while the alga’s population remained virtually constant. It seemed plausible that this unexpected result was due to changes in the relative abundances of at least two algal genotypes: one type more palatable to the rotifer predator and one less so. The authors reasoned that when rotifers became abundant, loss of the more palatable prey genotype might be compensated for by growth of the less palatable type, which no longer had to compete for access to nutrients. The numbers of the unpalatable algal type might grow large and, since it was unpalatable, cause the rotifer population to decline, giving advantage again to the more competitive but also more palatable genotype. As a test, they constructed a mathematical model that included terms for prey abundance, palatability, nutrient competition ability, birth rates, and other variables in the system, and found that it predicted that the two algal genotypes could exhibit exactly the observed population behavior when the fitness cost to the algae of being unpalatable was low. Furthermore, the model predicted a similar result for sexually reproducing species, not just asexual ones such as the alga. Low cost of defense against consumption is seen not only in the algae studied by Yoshida and colleagues, but is a widespread observation in many plant–herbivore interactions. Cryptic cycling: the rotifer Brachionus exhibits regular cycles in abundance, but the alga Chlorella, on which it feeds, does not—except in its genotype frequencies. The same occurs between the phage T4 and bacteria. While results from the model were encouraging, the authors did not have direct genotype data from the alga to back it up. Instead, they turned to another pair of interacting species, the bacterium Escherichia coli and the phage virus T4. These experiments used two strains of E. coli, one of which was resistant to attack by the phage and also carried an easily measured genetic marker. Again, they observed a relatively constant total bacterial population in the face of wide swings in phage abundance and confirmed that the population of the vulnerable bacterial strain showed a typical predator–prey cycle with the phage. In one experiment with only a susceptible strain but in which a spontaneous mutation arose to confer resistance, the total bacterial population ceased to oscillate and again stabilized. The authors call this pattern of predator–prey population changes “cryptic dynamics,” because the rapid change in relative genotype frequency in the prey masks the strong interaction between the two species. They predict that such a pattern may occur when the prey species is genetically diverse (as is true almost everywhere outside the laboratory), when the better defended (less palatable) genotype is also a poorer competitor for nutrients, and when the cost of defense is low. The implications of this prediction for understanding natural communities are extensive, the authors believe, since the conditions they propose may occur in a large fraction of trophic interactions. In such cases, they argue, lack of population co-oscillations cannot be taken as evidence that trophic interactions are weak: in other words, when it comes to population dynamics, absence of evidence is not evidence of absence.

Most corals may not change their symbionts

Many corals (stony corals and octo- corals) rely on their symbiotic algae (zooxanthellae) for survival. Under stress, zooxanthellae are ex- pelled, resulting in coral bleaching. The hypothesis that corals may survive climate change by ex- changing algal types is shown here to be potentially applicable only to a minority of corals. Data on 442 coral species from 43 studies reveal that only a few coral species may be able to change their symbionts. The ability to change symbionts seems to be linked to whether a coral species can host multiple zooxanthella clades, either at different depths on the same reef, on different reefs or at different geographic locations, or concurrently within the same colony. The combined data set shows that only 23% of coral species host multiple zoo- xanthella clades. Most coral species (77%) exhibit fidelity to a narrow subset of a single zooxanthella clade, some even to specific algal genotypes within a clade. These specific algal genotypes in coral species hosting a single algal clade do not change over time. Furthermore, no algal change occurs when a coral colony is either transplanted to differ- ent environments, or subjected to stressors such as disease or increased temperatures. For the majority of corals, therefore, algal switching does not appear to occur. These coral species will survive only if the existing host-symbiont combination withstands the changing conditions. If climate warming con- tinues, coral reefs may undergo a change in bio- diversity such that only a subset of symbiotic corals may persist.