THE EVOLUTION OF PARASITES FROM THEIR HOSTS: A CASE STUDY IN THE PARASITIC RED ALGAE

Morphological similarities of many parasites and their hosts have led to speculation that some groups of plant, animal, fungal, and algal parasites may have evolved directly from their hosts. These parasites, which have been termed adelphoparasites in the botanical literature, and more recently, agastoparasites in the insect literature, may evolve monophyletically from one host and radiate secondarily to other hosts or, these parasites may arise polyphyletically, each arising from its own host. In this study we compare the internal transcribed spacer regions of the nuclear ribosomal repeats of species and formae specialis (host races) included in the red algal parasite genus Asterocolax with its hosts, which all belong to the Phycodrys group of the Delesseriaceae and with closely related nonhost taxa of the Delesseriaceae. These analyses reveal that species of Asterocolax have evolved polyphyletically. Asterocolax erythroglossi from the North Atlantic host Erythroglossum laciniatum appears to have evolved from its host, whereas taxa included in the north Pacific species Asterocolax gardneri have had two independent origins. Asterocolax gardneri from the host Polyneura latissima probably arose directly from this host. In contrast, all other A. gardneri formae specialis appear to have originated from either Phycodrys setchellii or P. isabelliae and radiated secondarily onto other closely related taxa of the Phycodrys group, including Nienburgia andersoniana and Anisocladella pacifica. Gamete crossing experiments confirm that A. gardneri from each host is genetically isolated from both its host, and from other A. gardneri and their hosts. Cross-infection experiments reveal that A. gardneri develops normally only on its natural host, although some abberrant growth may occur on alternate hosts. The ability of red algal parasites to radiate secondarily to other red algal taxa, where they may become isolated genetically and speciate, suggests that this process of speciation is not a “genetic dead end” but one that may give rise to related clusters of parasite species.     

Comparative studies of photosynthetic capacity in three pigmented red algal parasites: Chlorophyll a concentrations and PAM fluorometry measurements

Over 100 species of red algae have been described as parasites on other red algae, but the majority show some degree of pigmentation. This raises the question of their parasitic status, especially their abilities to photosynthesize and their dependence on their host for fixed carbon. Are they considered parasites only based on morphological characters, for example, reduced size and secondary pit connection to the host? Translocation of nutrients from host to parasite have been shown for very few red algal parasites, and these were mostly unpigmented. This study investigated three pigmented red algal parasites (Rhodophyllis parasitica, Vertebrata aterrimophila and Pterocladiophila hemisphaerica) from New Zealand. We quantified their chlorophyll a content and also measured their PSII capacity using PAM fluorometry. All three parasites contained chlorophyll a. The parasites Rhodophyllis parasitica and Vertebrata aterrimophila were not able to photosynthesize and must therefore be fully nutritional dependent on their host. The parasite Pterocladiophila hemisphaerica was able to photosynthesize independently, but based on molecular characteristics we suggest that it relies on the host plastid to do photosynthesis. Our results support the parasitic status of all three species and highlights the necessity of more studies investigating the differences in host dependency in red algal parasites.     

Halogenating activities detected in Antarctic macroalgae

 Halogenating activities were determined in samples of 18 cultivated species of brown, red and green macroalgae from the Antarctic. Activities for the halogenating organic compounds with bromide, iodide and chloride were found. Investigated red algae (rhodophytes) showed higher brominating and iodinating activities compared to brown (phaeophytes) and green (chlorophytes) algae. The highest brominating and iodinating activities were measured in the red algae Plocamium cartilagineum (1.11±0.01 U g^-1 wet algal weight and 0.18 U g^-1 wet algal weight, respectively) and Myriogramme mangini (3.62±0.17 U g^-1 wet algal weight and 4.5 U g^-1 wet algal weight, respectively). Chlorinating activities were detected in the red alga Plocamium cartilagineum only (0.086 U g^-1 wet algal weight). Received: 12 February 1996/Accepted: 20 June 1996     

The ghost plastid of Choreocolax polysiphoniae

Parasitism has evolved innumerable times among eukaryotes. Red algal parasites alone have independently evolved over 100 times. The accepted evolutionary paradigm proposes that red algal parasites arise by first infecting a close relative and over time diversifying and infecting more distantly related species. This provides a natural evolutionary gradient of relationships between hosts and parasites that share a photosynthetic common ancestor. Upon infection, the parasite deposits its organelles into the host cell and takes over, spreading through cell‐cell connections. Microscopy and molecular studies have demonstrated that the parasites do not maintain their own plastid, but rather abscond with a dedifferentiated host plastid as they pack up spores for dispersal. We sequenced a ~90 kb plastid genome from the parasite Choreocolax polysiphoniae, which has lost genes for light harvesting and photosynthesis. Furthermore, the presence of a native C. polysiphoniae plastid indicates that not all red algal parasites follow the same evolutionary pathway to parasitism. Along with the 167 kb plastid genome of its host, Vertebrata lanosa, these plastids are the first to be sequenced from the Ceramiales.     

A PHYLOGENETIC STUDY OF PARASITIC GENERA PLACED IN THE FAMILY CHOREOCOLACACEAE (RHODOPHYTA)1

Red algal parasites are common and have a unique type of development in which parasite nuclei are transferred to host cells and “control” host cell development. Previous phylogenetic studies have concentrated on parasites closely related to their hosts, termed adelphoparasites. A second set of parasites, usually classified in a different family or tribe from their host, termed alloparasites, have not been studied phylogenetically. This study concentrates on the wholly parasitic family, the Choreocolacaceae (Gigartinales). Using small subunit rDNA sequence data, we found that all the parasites studied are within the same family as their host. Our data support the placement of Holmsella, species of which parasitize Gracilaria and Gracilariopsis, in the order Gracilariales and suggest that Holmsella is an old parasitic genus. Most other species of the Choreocolacaceae parasitize species of the Rhodomelaceae. The one exception is the hyperparasitism between Harveyella mirabilis (Reinsch) F. Schmitz et Reinke (Rhodomelaceae) and the parasite Gonimophyllum skottsbergii Setchell (Delesseriaceae). The parasites Bostrychiocolax australis Zuccarello et West and Dawsoniocolax bostrychiae (Joly et Yamaguishi‐Tomita) Joly et Yamaguishi‐Tomita are placed within the tribe Bostrychiae as are their hosts. Harveyella mirabilis has a single origin and has switched hosts several times during its passage between the Atlantic and Pacific Oceans. Evidence does not support the continued recognition of the family Choreocolacaceae. Our results also indicate that the distinction between adelphoparasites and alloparasites is unwarranted, with a continuum between newly evolved parasites closely related to their hosts and parasites less closely related to their hosts.     

Fate of Parasite and Host Organelle DNA during Cellular Transformation of Red Algae by Their Parasites

The transfer of a nucleus into a cytoplasm of a genetically foreign cell and its subsequent multiplication in the cytoplasm of this cell characterize most parasitic red algal species and their interactions with specific red algal hosts. Nuclei enter the host's cytoplasm upon cell fusion of parasite and host cell; here, they replicate, are spread to contiguous host cells, and ultimately are packaged into spores that reinfect other host thalli. In this study, we examined whether the proplastids and mitochondria that occur in these red algal adelphoparasites are acquired from their host or whether they are unique to the parasite and are brought into the host along with the parasite nucleus. To establish their origins and fates, plastid and mitochondrial restriction fragment length polymorphisms (RFLPs) of parasite cells were compared with those of their host plastid and mitochondrial DNA in three host and parasite pairs. For plastids, no RFLP differences were found between hosts and parasites, supporting an earlier conclusion, based on microscopic studies, that the proplastids of parasites are acquired from their hosts. For mitochondria, characteristic RFLP differences were detected between host and parasite for two of the pairs of species but not for the third. Evidence of the evolutionary difference between hosts and their parasites was shown by RFLP differences between nuclear ribosomal repeat regions.     

Molecular phylogenetics supports a clade of red algal parasites retaining native plastids: taxonomy and terminology revised

Parasitism is a life strategy that has repeatedly evolved within the Florideophyceae. Historically, the terms adelphoparasite and alloparasite have been used to distinguish parasites based on the relative phylogenetic relationship of host and parasite. However, analyses using molecular phylogenetics indicate that nearly all red algal parasites infect within their taxonomic family, and a range of relationships exist between host and parasite. To date, all investigated adelphoparasites have lost their plastid, and instead, incorporate a host‐derived plastid when packaging spores. In contrast, a highly reduced plastid lacking photosynthesis genes was sequenced from the alloparasite Choreocolax polysiphoniae. Here we present the complete Harveyella mirabilis plastid genome, which has also lost genes involved in photosynthesis, and a partial plastid genome from Leachiella pacifica. The H. mirabilis plastid shares more synteny with free‐living red algal plastids than that of C. polysiphoniae. Phylogenetic analysis demonstrates that C. polysiphoniae, H. mirabilis, and L. pacifica form a robustly supported clade of parasites, which retain their own plastid genomes, within the Rhodomelaceae. We therefore transfer all three genera from the exclusively parasitic family, Choreocolacaceae, to the Rhodomelaceae. Additionally, we recommend applying the terms archaeplastic parasites (formerly alloparasites), and neoplastic parasites (formerly adelphoparasites) to distinguish red algal parasites using a biological framework rather than taxonomic affiliation with their hosts.     

Development of the red algal parasite Vertebrata aterrimophila sp. nov. (Rhodomelaceae,Ceramiales) from New Zealand

Parasitic red algae grow only on other red algae and have over 120 described species. Developmental studies in red algal parasites are few, although they have shown that secondary pit connections formed between parasite and host and proposed that this was an important process in successful parasitism. Furthermore, it was recorded that the transfer of parasite nuclei by these secondary pit connections led to different host cell effects. We used developmental studies to reconstruct early stages and any host cell effects of a parasite on Vertebrata aterrima. A mitochondrial marker (cox1) and morphological observations (light and fluorescence microscopy) were used to describe this new red algal parasite as Vertebrata aterrimophila sp. nov. Early developmental stages show that a parasite spore connects via secondary pit connections with a pericentral host cell after cuticle penetration. Developmental observations revealed a unique connection cell that grows into a ‘trunk-like’ structure. Host cell transformation after infection by the parasite included apparent increases in both carbohydrate concentrations and nuclear size, as well as structural changes. Analyses of molecular phylogenies and reproductive structures indicated that the closest relative of V. aterrimophila is its host, V. aterrima. Our study shows a novel developmental parasite stage (‘trunk-like’ cell) and highlights the need for further developmental studies to investigate the range of developmental patterns and host effects in parasitic red algae.     

THE ROLE OF SECONDARY PIT CONNECTIONS IN RED ALGAL PARASITISM1

Secondary pit connections are common between cells of hosts and parasites in the widespread phenomenon of red algal parasitism. The DNA-specific fluorochrome 4′,-6-diamidino-2-phenylindole (DAPI) reveals that in host-parasite secondary pit connection (SPC) formation between the parasitic red alga Choreocolax polysiphoniae and its host Polysiphonia confusa, a nucleus and other cytoplasmic components of the parasite are delivered into the cytoplasm of a host cell. Host cells receive large numbers of parasite nuclei and these, apparently arrested in G¹, are maintained intact in host cells for periods of several weeks. Within these enlarged, differentiated cells, starch accumulates and cytoplasmic organelles proliferate as the central vacuole decreases in size. Host nuclear DNA synthesis is stimulated in the infected host cell, resulting in an increase in the number of host nuclei, or an increase in DNA in each of the existing host nuclei (i.e. somatic polyploidy). Occasionally, infected host cells will recommence division and engender a new host branch. Microspectrofluorometry of nuclear DNA quantitatively confirms not only the identity and transfer of parasite nuclei to host cells, but also the transfer of parasite nuclei to other parasite cells. Measurements also reveal that the single nucleus of Choreocolax becomes progressively more polyploid as cells become larger and more highly differentiated. Secondary pit connection formation between Choreocolax and Polysiphonia provides the mechanism for the transfer of parasite genetic information (via the parasite nucleus and cytoplasm) into the host. The parasite nuclei may thereby control and redirect the physiology of the host for the benefit of the parasite.     

The ecology and phylogeny of oomycete infections in Asplanchna rotifers

1. Recently, the potential for parasites to influence the ecology and evolution of their zooplankton hosts has been the subject of increasing study. However, most research to date has focussed on Daphnia hosts, and the potential for parasites to influence other zooplankton taxa remains largely unstudied. 2. During routine sampling of zooplankton in a eutrophic lake, we observed that the rotifer Asplanchna girodi was often infected with a parasitic oomycete. Epidemics of this parasite occurred frequently, with three separate events in a single year. Prevalence at peak infection ranged from 29 to 41% and epidemics lasted from 17 to 56 days. Our data indicate that high densities of the host population are required for epidemics to occur. 3. Our morphological and molecular analyses suggest that this parasite is in the genus Pythium. Most Pythium spp. are plant pathogens, but our study supports recent work on Daphnia, suggesting that Pythium spp. are also important parasites of zooplankton. 4. As the parasite in this study was recalcitrant to cultivation, we developed an alternative method to verify its identity. Our approach used quantitative PCR to show that the ribosomal sequences identified increased with increasing density of infected hosts and, thus, were associated with the parasite. This approach should be generally applicable to other plankton parasites that are difficult to cultivate outside their hosts. 5. Infections significantly reduced host fecundity, lifespan and population growth rate. As a result of the virulence of this parasite, it is likely to influence the population ecology and evolution of its Asplanchna host, and may be a useful model system for studies on host–parasite coevolutionary dynamics.     

THE INFLUENCE OF HOST DEMOGRAPHY ON THE EVOLUTION OF VIRULENCE OF A MICROSPORIDIAN GUT PARASITE

It is predicted that host exploitation should evolve to maximize parasite fitness and that virulence (= parasite-induced host mortality) evolves along with the rate of host exploitation. If the life expectancy of a parasite is short, it is expected to evolve a higher rate of host exploitation and therefore higher virulence because the penalty to the parasite for killing the host is reduced. We tested this hypothesis by keeping for 14 months the horizontally transmitted microsporidian parasite Glugoides intestinalis in mono-clonal host cultures (Daphnia magna) under conditions of high and low host background mortality. High host mortality, and thus parasite mortality, was achieved by replacing weekly 70–80% of all hosts in a culture with uninfected hosts from stock cultures (Replacement lines). In the low-mortality treatment no replacement took place. Contrary to our expectation, parasites from the Replacement lines evolved a lower within-host growth rate and virulence than parasites from the Nonreplacement lines. Across lines we found a strong positive correlation between within-host growth rate and virulence. We did further experiments to answer the question why our data did not support the predictions. Sporophorous vesicles (SVs, spore clusters) were smaller in doubly infected than in singly infected host-gut cells, indicating that competition within cells bears costs for the parasite. Due to our experimental protocol, the average life span of infections had been much higher in the Nonreplacement lines. Since the number of parasites inside a host increases with the time since infection, long-lasting infections led to high frequencies of multiply infected host-gut cells. Therefore, we speculated that within-cell competition was more severe in the Nonreplacement lines and may have led to selection for accelerated within-host growth. SVs in the Nonreplacement lines were indeed significantly larger. Our results point out that single-factor explanations for the evolution of virulence can lead to wrong predictions and that multiple infections are an important factor in virulence evolution.     

BIOGEOGRAPHY AND ECOLOGY OF THE KELP/RED ALGAL SYMBIOSIS

A kelp/red algal symbiosis is described from nature based on extensive collections from the San Juan Islands, Washington. Kelp gametophytes were found as endophytes in the cell walls of seventeen species of red algae in three different kelp communities. Host red algae were mostly filamentous (e.g., Pleonosporium vancouverianum) or polysiphonous (e.g. Polysiphonia paniculata). The kelp gametophytes completed vegetative and reproductive development in the hosts with gametangia formed at the host surface and with sporophytes up to several mm in height being produced while still attached to the host. To date, none of the kelp gametophytes from nature have been identified to genus or species, although the gametophyte of Nereocystis luetkeana is a potential candidate for the symbiosis. Preliminary observations from Nova Scotia and the Isle of Man have not found the association in the Atlantic Ocean. Laboratory studies in Korea successfully reconstructed the symbiosis in the red alga Aglaothamnion oosumiense using zoospores of Undaria pinnatifida but not Laminaria religiosa. Here we outline the development of the symbiosis and discuss the potential adaptive significance of the kelp/red algal interaction.     

Gene-rich plastid genomes of two parasitic red algal species,Laurencia australis and L. verruciformis (Rhodomelaceae,Ceramiales), and a taxonomic revision of Janczewskia

Parasitic red algae are an interesting system for investigating the genetic changes that occur in parasites. These parasites have evolved independently multiple times within the red algae. The functional loss of plastid genomes can be investigated in these multiple independent examples, and fine-scale patterns may be discerned. The only plastid genomes from red algal parasites known so far are highly reduced and missing almost all photosynthetic genes. Our study assembled and annotated plastid genomes from the parasites Janczewskia tasmanica and its two Laurencia host species (Laurencia elata and one unidentified Laurencia sp. A25) from Australia and Janczewskia verruciformis, its host species (Laurencia catarinensis), and the closest known free-living relative (Laurencia obtusa) from the Canary Islands (Spain). For the first time we show parasitic red algal plastid genomes that are similar in size and gene content to free-living host species without any gene loss or genome reduction. The only exception was two pseudogenes (moeB and ycf46) found in the plastid genome of both isolates of J. tasmanica, indicating potential for future loss of these genes. Further comparative analyses with the three highly reduced plastid genomes showed possible gene loss patterns, in which photosynthetic gene categories were lost followed by other gene categories. Phylogenetic analyses did not confirm monophyly of Janczewskia, and the genus was subsumed into Laurencia. Further investigations will determine if any convergent small-scale patterns of gene loss exist in parasitic red algae and how these are applicable to other parasitic systems.     

HOST SPECIFICITY IN THE RED ALGAL PARASITES BOSTRYCHIOCOLAX AUSTRALIS AND DAWSONIOCOLAX BOSTRYCHIAE (CHOREOCOLACACEAE,RHODOPHYTA)1

The determinants of host specificity, which are poorly understood in red algal parasites, were studied in the red algal parasites Bostrychiocolax australis Zuccarello et West and Dawsoniocolax bostrychiae (Joly et Yamaguishi-Tomita) Joly et Yamaguishi-Tomita. Culture studies were performed to determine host range, sites of host resistance, and genetics of transmission of resistance. Both species parasitize Bostrychia radicans (Montagne) Montagne, whereas Bostrychiocolax australis also parasitizes Bostrychia moritziana (Sonder ex Kützing) J. Agardh and Stictosiphonia kelanensis (Grunow ex Post) R. J. King et Puttock. Isolates of B. radicans resistant to both parasites were found worldwide, often within the same population as susceptible isolates. On resistant Bostrychia species and isolates, specificity was manifested at three stages: 1) host penetration, in which the spore germ peg failed to penetrate the host cuticle/wall; 2) parasite–host cell fusion, in which the fusion cell died and the parasite died; and 3) growth, in which parasites grew but soon died; parasites rarely reproduced and infections did not continue in culture. Resistance to parasite infection was usually transmitted as a dominant trait and did not segregate as a single locus during meiosis. In certain crosses, transmission of resistance was non-mendelian.     

MOLECULAR PHYLOGENY AND EVOLUTION OF RED ALGAL PARASITES: A CASE STUDY OF BENZAITENIA,JANCZEWSKIA, AND ULULANIA (CERAMIALES)1

A molecular phylogenetic study of red algal parasites commonly found in the Northwestern Pacific and the Hawaiian Islands was undertaken. Four species, Benzaitenia yenoshimensis Yendo, Janczewskia hawaiiana Apt, J. morimotoi Tokida, and Ululania stellata Apt et Schlech (Ceramiales), are parasitic on rhodomelacean species belonging to the tribes Chondrieae and Laurencieae. Although Janczewskia and Ululania are classified in the same tribes as their host species, the taxonomic placement of Benzaitenia has been controversial. To infer the phylogenetic positions of these parasites and to clarify the relationships between the parasites and their hosts, phylogenetic analyses of partial nuclear SSU and LSU rRNA genes and the cox1 gene were performed. The SSU rRNA gene analyses clearly show that both Janczewskia species are positioned within the Laurencia s. str. clade with their host species, while Benzaitenia and Ululania are placed in the Chondrieae clade. According to these analyses, J. hawaiiana and U. stellata are not sister to their current hosts; in contrast, B. yenoshimensis and J. morimotoi are closely related to their current hosts. These data suggest that J. hawaiiana and U. stellata have likely evolved from species other than their current hosts and have switched hosts at some point in their evolutionary history. Likelihood ratio tests do not support the monophyly of J. hawaiiana and J. morimotoi, suggesting multiple origins of parasitism within Laurencia s. str.     

SUBOPTIMAL VIRULENCE OF AN INSECT-PARASITIC NEMATODE

Recent considerations of parasite virulence have focused on the adverse effects that parasites can have on the survival of their hosts. Many parasites, however, reduce host fitness by an equally deleterious but different means, by causing partial or complete sterility of their hosts. A model of optimal parasite virulence is developed in which a quantity of host resources can be allocated to either host or parasite reproduction. Increases in parasite reproduction thus cause reductions in host fertility. The model shows that under a wide variety of ecological conditions, such parasites should completely sterilize their hosts. Only when opportunities for horizontal transmission are very limited should the parasites appropriate less than all of a host's reproductive resources. Field and laboratory evidence shows that the nematode parasite Howardula aoronymphium is relatively avirulent to one of its principal host species, Drosophila falleni, whereas it is much more virulent to D. putrida and D. neotestacea, suggesting that there may be substantial vertical transmission in D. falleni. However, epidemiological studies in the field and laboratory assays of host specificity strongly suggest that the three host species share a single parasite pool in natural populations, indicating that parasites in all three host species experience high levels of horizontal transmission. Thus, the low virulence of H. aoronymphium to D. falleni is not consistent with the model of optimal parasite virulence. It is proposed that this suboptimal virulence in D. falleni is a consequence of populations of H. aoronymphium being selected to exploit simultaneously several different host species. As a result, virulence may not be optimal in any one host. One must, therefore, consider the full range of host species in assessing a parasite's virulence.     

MAGPIE HOST MANIPULATION BY GREAT SPOTTED CUCKOOS: EVIDENCE FOR AN AVIAN MAFIA?

Why should the hosts of brood parasites accept and raise parasitic offspring that differ dramatically in appearance from their own? There are two solutions to this evolutionary enigma. (1) Hosts may not yet have evolved the capability to discriminate against the parasite, or (2) parasite-host systems have reached an evolutionary equilibrium. Avian brood parasites may either gain renesting opportunities or force their hosts to raise parasitic offspring by destroying or preying upon host eggs or nestlings following host ejection of parasite offspring. These hypotheses may explain why hosts do not remove parasite offspring because only then will hosts avoid clutch destruction by the cuckoo. Here we show experimentally that if the egg of the parasitic great spotted cuckoo Clamator glandarius is removed from nests of its magpie Pica pica host, nests suffer significantly higher predation rates than control nests in which parasite eggs have not been removed. Using plasticine model eggs resembling those of magpies and observations of parasites, we also confirm that great spotted cuckoos that have laid an ejected egg are indeed responsible for destruction of magpie nests with experimentally ejected parasite eggs. Cuckoos benefit from destroying host offspring because they thereby induce some magpies to renest and subsequently accept a cuckoo egg.     

TEMPERATURE REQUIREMENTS FOR GROWTH AND SURVIVAL OF ANTARCTIC RHODOPHYTA1

The temperature requirement for growth and the upper survival temperatures (USTs) of 15 Antarctic red algal species collected on King George Island (South Shetland Islands) and Signy Island (South Orkney Islands) were determined. Two groups with different temperature requirements were identified. 1) A “eurythermal” group includes Rhodymenia subantarctica, Phyllophora ahnfeltioides, Gymnogongrus antarcticus, and Rhodochorton purpureum, growing between 0° and 10°C with optimum values at (0°) 5°(l0°)C. The USTs of these species and of Porphyra endiviifolium, Delesseria lancifolia, and Bangia atropurpurea were between 22° and 16°C. These species survived temperatures in a similar range as most endemic Arctic or Arctic/cold-temperate species but exhibited a lower temperature demand for growth, suggesting an earlier contact with low temperatures than Arctic species. 2) A stenothermal group includes Pantoneura plocamioides, Myriogramme mangini, Ballia callitricha, Phyllophora antarctica, Gigartina skottsbergii, Georgiella confluens, and Plocamium cartilagineum growing at 0° or ≤5°C with optimum values at 0° or 5°C. The USTs of these species and of Phycodrys austrogeorgica were between 14° and 7°C. The species of this group must have had an even earlier contact with the Antarctic cold-water environment than species of the “eurythermal” group. Gigartina skottsbergii, Georgiella confluens, Plocamium cartilagineum, and Pantoneura plocamioides were probably exposed longer to low temperatures than the other species of this group or Antarctic green and brown algae because they show the lowest temperature requirements so far determined in seaweeds. The results are discussed in the context of present local temperature regimes at the localities where the isolates were collected. Moreover, an attempt was made to explain the geographic distribution of individual species by the temperature requirements determined in this study. Only a few of the distribution limits are determined by temperature growth and/or survival characteristics. In many species (Rhodymenia subantarctica, Ballia callitricha, Gigartina skottsbergii, Bangia atropurpurea, Rhodochorton purpureum, and Plocamium cartilagineum), the development of temperature ecotypes is evident.     

EVOLUTIONARY ANALYSES OF THE NUCLEAR‐ENCODED PHOTOSYNTHETIC GENE psbO FROM TERTIARY PLASTID‐CONTAINING ALGAE IN DINOPHYTA1

Although the dinophytes generally possess red‐algal‐derived secondary plastids, tertiary plastids originating from haptophyte and diatom ancestors are recognized in some lineages within the Dinophyta. However, little is known about the nuclear‐encoded genes of plastid‐targeted proteins from the dinophytes with diatom‐derived tertiary plastids. We analyzed the sequences of the nuclear psbO gene encoding oxygen‐evolving enhancer protein from various algae with red‐algal‐derived secondary and tertiary plastids. Based on our sequencing of 10 new genes and phylogenetic analysis of PsbO amino acid sequences from a wide taxon sampling of red algae and organisms with red‐algal‐derived plastids, dinophytes form three separate lineages: one composed of peridinin‐containing species with secondary plastids, and the other two having haptophyte‐ or diatom‐derived tertiary plastids and forming a robust monophyletic group with haptophytes and diatoms, respectively. Comparison of the N‐terminal sequences of PsbO proteins suggests that psbO genes from a dinophyte with diatom‐derived tertiary plastids (Kryptoperidinium) encode proteins that are targeted to the diatom plastid from the endosymbiotic diatom nucleus as in the secondary phototrophs, whereas the fucoxanthin‐containing dinophytes (Karenia and Karlodinium) have evolved an additional system of psbO genes for targeting the PsbO proteins to their haptophyte‐derived tertiary plastids from the host dinophyte nuclei.     

Temporally consistent species differences in parasite infection but no evidence for rapid parasite‐mediated speciation in Lake Victoria cichlid fish

Parasites may have strong eco‐evolutionary interactions with their hosts. Consequently, they may contribute to host diversification. The radiation of cichlid fish in Lake Victoria provides a good model to study the role of parasites in the early stages of speciation. We investigated patterns of macroparasite infection in a community of 17 sympatric cichlids from a recent radiation and 2 older species from 2 nonradiating lineages, to explore the opportunity for parasite‐mediated speciation. Host species had different parasite infection profiles, which were only partially explained by ecological factors (diet, water depth). This may indicate that differences in infection are not simply the result of differences in exposure, but that hosts evolved species‐specific resistance, consistent with parasite‐mediated divergent selection. Infection was similar between sampling years, indicating that the direction of parasite‐mediated selection is stable through time. We morphologically identified 6 Cichlidogyrus species, a gill parasite that is considered a good candidate for driving parasite‐mediated speciation, because it is host species‐specific and has radiated elsewhere in Africa. Species composition of Cichlidogyrus infection was similar among the most closely related host species (members of the Lake Victoria radiation), but two more distantly related species (belonging to nonradiating sister lineages) showed distinct infection profiles. This is inconsistent with a role for Cichlidogyrus in the early stages of divergence. To conclude, we find significant interspecific variation in parasite infection profiles, which is temporally consistent. We found no evidence that Cichlidogyrus‐mediated selection contributes to the early stages of speciation. Instead, our findings indicate that species differences in infection accumulate after speciation.