Parasite escape through trophic specialization in a species flock

Adaptive radiation occurs when species diversify rapidly to occupy an array of ecological niches. As opportunities for parasite infection and transmission may greatly vary among these niches, adaptive radiation is expected to be associated with a turnover of the parasite community. As major agents of natural and sexual selection, parasites may play a central role in host diversification. The study of parasite turnover may thus be of general relevance and could significantly improve our understanding of adaptive radiation. In this study, we examined the parasite faunas of eleven species belonging to the tribe Tropheini, one of several adaptive radiations of cichlid fishes in Lake Tanganyika. The most parsimonious ancestral foraging strategy among the Tropheini is relatively unselective substrate browsing of aufwuchs. Several lineages evolved more specialized foraging strategies, such as selective combing of microscopic diatoms or picking of macro‐invertebrates. We found that representatives of these specialized lineages bear reduced infection with food‐web‐transmitted acanthocephalan helminths, but not with parasites with a direct life cycle. Possibly, the evolution of selective foraging strategies entailed reduced ingestion of intermediate invertebrate hosts of acanthocephalans. We conclude that some species belonging to the Tropheini virtually escape acanthocephalan infection as a by‐product of trophic specialization.     

The evolution of ecological specialization across the range of a broadly distributed marine species

Ecological specialization is an important engine of evolutionary change and adaptive radiation, but empirical evidence of local adaptation in marine environments is rare, a pattern that has been attributed to the high dispersal ability of marine taxa and limited geographic barriers to gene flow. The broad-nosed pipefish, Syngnathus typhle, is one of the most broadly distributed syngnathid species and shows pronounced variation in cranial morphology across its range, a factor that may contribute to its success in colonizing new environments. We quantified variation in cranial morphology across the species range using geometric morphometrics, and tested for evidence of trophic specialization by comparing individual-level dietary composition with the community of prey available at each site. Although the diets of juvenile pipefish from each site were qualitatively similar, ontogenetic shifts in dietary composition resulted in adult populations with distinctive diets consistent with their divergent cranial morphology. Morphological differences found in nature are maintained under common garden conditions, indicating that trophic specialization in S. typhle is a heritable trait subject to selection. Our data highlight the potential for ecological specialization in response to spatially variable selection pressures in broadly distributed marine species.     

Temporal stability of individual feeding specialization may promote speciation

1.  Inter-individual differences in trophic behaviour are considered important in the disruptive selection process for resource specialization and may represent an early phase in the evolution of polymorphism and adaptive radiation. Here, we provide evidence of high stability of individual trophic niches of a fish predator from a 15-year study.
2.  Individual resource specialization was investigated by combining data from analyses of stomach contents (recent trophic niche), trophically transmitted parasites (long-term niche) and trophic morphology (niche adaptations) from single specimens of a postglacial fish (Arctic charr) population sampled from contrasting pelagic and littoral habitats.
3.  Based on the relationships between morphology, parasites and diet, high inter-individual temporal consistency of narrow niches (zooplanktivorous vs . benthivorous) was evident through the ontogeny of the charr, indicating low degree of switching both in habitat utilization and feeding strategy of individual fish. Co-occurrence of differently specialized behavioural phenotypes was sustained over multiple generations.
4.  The stable long-term habitat and feeding specializations may represent an important initial step in an adaptive radiation process, and our findings suggest a case of sympatric speciation into two incipient forms diverging along the littoral–pelagic resource axis.     

Evolutionary Relationships of the Limnochromini, a Tribe of Benthic Deepwater Cichlid Fish Endemic to Lake Tanganyika, East Africa

Lake Tanganyika harbors an enormous diversity of cichlid fish that stem from eight distinct ancestral lineages, which colonized the lake after its formation 9 to 12 million years ago. Six of twelve currently described tribes are assigned to the H-lineage, an assemblage of exclusively mouthbrood-ing cichlids, all of which evolved during a short period of time during the course of the primary radiation of lacustrine species. Our study focuses on the deepwater tribe Limnochromini, comprising bi-parental mouthbrooders, and is based on phylogenetic analysis of two mitochondrial gene segments. We confirm the polyphyletic origin of the Limnochromini as they are defined to date, in that Gnathochromis pfefferi is placed among the Tropheini, whereas the genus Benthochromis is presented as an independent lineage. The remaining nine species were unambiguously resolved as monophyletic and should be redefined as the tribe Limnochromini. Concerning generic assignments, the genus Greenwoodochromis appeared as monophyletic, Limnochromis as paraphyletic, and the genera Reganochromis and Baileychromis as monophyletic sister genera. The linearized tree analysis and the comparison of average sequence divergences to that of the remaining tribes of the H-lineage revealed a relatively recent but simultaneous proliferation of the Limnochromini, suggesting that the same environmental changes triggered the radiation of particular deepwater, benthic, pelagic, and littoral lineages. By using a preliminary calibration of a molecular clock based on gamma-corrected amino acid distances of the NADH2 gene, the diversification of the Limnochromini could tentatively be dated to 2.9–3.5 MYA, coinciding with a period of aridification in East Africa between 2.5 and 3 MYA. The lack of geographic color morphs and the structural uniformity and resource scarcity of deepwater habitats suggest that competition and resource partitioning leading to differential trophic specialization promoted speciation within the Limnochromini, rather than an allopatric model.Reviewing Editor: Dr. Axel Meyer     

TESTING FOR ANCIENT ADAPTIVE RADIATIONS IN NEOTROPICAL CICHLID FISHES

Most contemporary studies of adaptive radiation focus on relatively recent and geographically restricted clades. It is less clear whether diversification of ancient clades spanning entire continents is consistent with adaptive radiation. We used novel fossil calibrations to generate a chronogram of Neotropical cichlid fishes and to test whether patterns of lineage and morphological diversification are congruent with hypothesized adaptive radiations in South and Central America. We found that diversification in the Neotropical cichlid clade and the highly diverse tribe Geophagini was consistent with diversity‐dependent, early bursts of divergence followed by decreased rates of lineage accumulation. South American Geophagini underwent early rapid differentiation in body shape, expanding into novel morphological space characterized by elongate‐bodied predators. Divergence in head shape attributes associated with trophic specialization evolved under strong adaptive constraints in all Neotropical cichlid clades. The South American Cichlasomatini followed patterns consistent with constant rates of morphological divergence. Although morphological diversification in South American Heroini was limited, Eocene invasion of Central American habitats was followed by convergent diversification mirroring variation observed in Geophagini. Diversification in Neotropical cichlids was influenced by the early adaptive radiation of Geophagini, which potentially limited differentiation in other cichlid clades.     

PHYLOGENY OF THE CONJUGATING GREEN ALGAE BASED ON CHLOROPLAST AND MITOCHONDRIAL NUCLEOTIDE SEQUENCE DATA1

The conjugating green algae represent a lineage of charophyte green algae known for their structural diversity and unusual mode of sexual reproduction, conjugation. These algae are ubiquitous in freshwater environments, where they are often important primary producers, but few studies have investigated evolutionary relationships in a molecular systematic context. A 109‐taxon data set consisting of three gene fragments (two from the chloroplast and one from the mitochondrial genome) was used to estimate the phylogeny of the genera of the conjugating green algae. Maximum likelihood (ML), maximum parsimony (MP), and Bayesian inference (BI) were used to estimate relationships from the 4,047 alignable nucleotides. This study confirmed the polyphyly of the Zygnemataceae and Mesotaeniaceae with respect to one another. The Peniaceae were determined to be paraphyletic, and two genera traditionally classified among the Zygnematales appear to belong to the lineage that gave rise to the Desmidiales. Six genera, Euastrum, Cosmarium, Cylindrocystis, Mesotaenium, Spondylosium, and Staurodesmus, were polyphyletic in this analysis. These findings have important implications for the evolution of structural characteristics in the group and will require some taxonomic changes. More work will be required to delineate lineages of Zygnematales in particular and to identify structural synapomorphies for some of the newly identified clades.     

Evolution of the tribe Tropheini from Lake Tanganyika: synchronized explosive speciation producing multiple evolutionary parallelism

One of the most surprising outcomes of recent molecular studies on cichlid fishes of the three Great East African Lakes Victoria, Malawi and Tanganyika, was the stunning rapidity of speciation and cladogenesis at early stages of adaptive radiation. Despite their rapid pace, speciation events were so far intuitively assumed to proceed in a bifurcating and tree-like fashion, even if they could not be resolved by gene phylogenies due to a lack of resolution. On the basis of phylogenetic analyses of the Tropheini, a lineage of endemic rock-dwelling cichlid fishes from Lake Tanganyika, we suggest a pathway of explosive speciation that accounts for a non-bifurcating manner of cladogenesis. This pattern is likely to be the result of the contemporaneous origin of a multitude of founder populations in geographically isolated rock habitats among which gene flow was interrupted simultaneously by a major change of the lake habitat in the form of a rapid rise of the lake level. As a consequence, all new species arising from that vicariance event must exhibit almost equal genetic distances to each other, within the scope of genetic diversity of the founder population(s), even if the actual processes of subsequent speciation and eco-morphological diversification followed independent routes. Our phylogeny also suggests a high frequency of parallel evolution of equivalent trophic specialization in the Tropheini. This phenomenon seems to be an inherent feature of this pathway of speciation, due to the action of similar selective forces on the same set of species colonizing isolated habitats of the same type. Explosive speciation via synchronization of genetic divergence triggered by rapid environmental changes seems to be particularly likely to occur at advanced stages of adaptive radiation, when species are already adapted to particular habitats and have a reduced ability for dispersal.     

Reassessment of the trophic position of Bullidae (Gastropoda: Cephalaspidea) and the importance of diet in the evolution of cephalaspidean gastropods

A review of the available data on the diet of species of Bullidae is presented. Their trophic level is reassessed through gut content analysis of worldwide species from various habitats. Gut contents were identified by light and scanning electron microscopy. The previous claims of omnivory and carnivory were not supported. Worldwide species of Bullidae feed preferentially on algae and secondarily on diatoms, and are therefore herbivorous. The influence of dietary specialization on the evolution of cephalaspidean gastropods was assessed by superimposing the diet onto a molecular family-level phylogeny. Herbivory was found to be the plesiomorphic condition, with carnivory having arisen independently two or three times. This evidence suggests that dietary specialization has played a major role in the adaptive radiation of the group.     

Rush hour at the Museum – Diversification patterns provide new clues for the success of figs (Ficus L., Moraceae)

Tropical rainforests harbour much of the earth's plant diversity but little is still known about how it evolved and why a small number of plant genera account for the majority. Whether this success is due to rapid turnover or constant evolution for these hyper-diverse plant genera is here tested for the species-rich genus Ficus L. (figs). The pan-tropical distribution of figs makes it an ideal study group to investigate rainforest hyper-diversification patterns. Using a recently published, dated and comprehensive phylogenetic hypothesis, we infer that figs are an old lineage that gradually accumulated species and exhibits very low extinction rates, which corresponds to the ‘museum model’ of evolution. Overall, no major significant shifts in evolutionary dynamics are detected, yet two shifts with lower probability are found. Hemi-epiphytism, monoecy, and active pollination are traits that possibly are associated with the hyper-diversity found in figs, making it possible for the plants to occupy new niches followed by extensive radiation over evolutionary time scales. Figs possess unique diversification patterns compared to other typical rainforest genera.     

Geographic host use variability and host range evolutionary dynamics in the phytophagous insect <Emphasis Type="Italic">Apagomerella versicolor</Emphasis> (Cerambycidae)

The high diversity of phytophagous insects has been explained by the tendency of the group towards specialization; however, generalism may be advantageous in some environments. The cerambycid Apagomerella versicolor exhibits intraspecific geographical variation in host use. In northern Argentina it is highly specialized on the herb Pluchea sagittalis (Asteraceae), while in central and southern areas it uses seven Asteraceae species. To study host species geographical variation from ecological and evolutionary perspectives, we investigated field host availability and use across a wide latitudinal range, and performed laboratory studies on insect oviposition preference and larval performance and mitochondrial DNA (mtDNA) variation in a phylogeographical framework. Geographic variation in host use was unrelated to host availability but was highly associated with laboratory oviposition preference, larval performance, and mtDNA variation. Genetic studies revealed three geographic races of A. versicolor with gene flow restriction and recent geographic expansion. Trophic generalism and oligophagy within A. versicolor seem to have evolved as adaptations to seasonal and spatial unavailability of the preferred host P. sagittalis in cooler areas of the species’ geographic range. No single genotype is successful in all environments; specialization may be advantageous in environments with uniform temporal and spatial host availability, while being a trophic generalist may provide an adaptive advantage in host-constrained environments.     

When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model

Conceptual models of adaptive radiation predict that competitive interactions among species will result in an early burst of speciation and trait evolution followed by a slowdown in diversification rates. Empirical studies often show early accumulation of lineages in phylogenetic trees, but usually fail to detect early bursts of phenotypic evolution. We use an evolutionary simulation model to assemble food webs through adaptive radiation, and examine patterns in the resulting phylogenetic trees and species' traits (body size and trophic position). We find that when foraging trade-offs result in food webs where all species occupy integer trophic levels, lineage diversity and trait disparity are concentrated early in the tree, consistent with the early burst model. In contrast, in food webs in which many omnivorous species feed at multiple trophic levels, high levels of turnover of species' identities and traits tend to eliminate the early burst signal. These results suggest testable predictions about how the niche structure of ecological communities may be reflected by macroevolutionary patterns.     

Trophic diversity in the evolution and community assembly of loricariid catfishes

ABSTRACT: BACKGROUND: The Neotropical catfish family Loricariidae contains over 830 species that display extraordinary variation in jaw morphologies but nonetheless reveal little interspecific variation from a generalized diet of detritus and algae. To investigate this paradox, we collected delta13C and delta15N stable isotope signatures from 649 specimens representing 32 loricariid genera (82 species) from 19 local assemblages distributed across South America. We calculated vectors representing the distance and direction of each specimen relative to the delta15N/delta13C centroid for its local assemblage, and then examined the evolutionary diversification of loricariids across assemblage isotope niche space by regressing the mean vector for each genus in each assemblage onto a phylogeny reconstructed from osteological characters. RESULTS: Loricariids displayed a total range of delta15N assemblage centroid deviation spanning 4.9per thousand, which is within the tissue-diet discrimination range known for Loricariidae, indicating that they feed at a similar trophic level and that delta15N largely reflects differences in their dietary protein content. Total range of delta13C deviation spanned 7.4per thousand, which is less than the minimum range reported for neotropical river fish communities, suggesting that loricariids selectively assimilate a restricted subset of the full basal resource spectrum available to fishes. Phylogenetic regression of assemblage centroid-standardized vectors for delta15N and delta13C revealed that loricariid genera with allopatric distributions in disjunct river basins partition basal resources in an evolutionarily conserved manner concordant with patterns of jaw morphological specialization and with evolutionary diversification via ecological radiation. CONCLUSIONS: Trophic partitioning along elemental/nutritional gradients may provide an important mechanism of dietary segregation and evolutionary diversification among loricariids and perhaps other taxonomic groups of apparently generalist detritivores and herbivores. Evolutionary patterns among the Loricariidae show a high degree of trophic niche conservatism, indicating that evolutionary lineage affiliation can be a strong predictor of how basal consumers segregate trophic niche space.     

Reconstruction of phylogenetic relationships within Grapsidae (Crustacea: Brachyura) and comparison of trans-isthmian versus amphi-atlantic gene flow based on mtDNA

Following taxonomic revisions in recent years, the originally large family Grapsidae MacLeay, 1838 has become a relatively small and morphologically homogeneous family in terms of adult and larval morphology. Most available molecular studies including more than one genus of the family have also suggested monophyly of the corresponding taxa. However, no single phylogenetic study has ever included all constituent genera of the Grapsidae. In the current study, a molecular phylogeny based on sequences of the mitochondrial 16S rRNA gene from all eight grapsid genera and 34 species is presented and suggests that up to four genera are not monophyletic. This is mainly due to the polyphyletic nature of the genus Pachygrapsus which can be found in six different lineages of the phylogeny, suggesting that the genus currently does not represent a single evolutionary lineage and is in need of taxonomic revision. Amphi-atlantic and trans-isthmian species pairs or populations in four genera are compared and reveal relatively constant and pronounced divergences across the Panama Isthmus as opposed to moderate divergences across the Atlantic Ocean, thereby suggesting occurrence of gene flow across the Atlantic Ocean during the past three million years.     

Trophic specialization influences the rate of environmental niche evolution in damselfishes (Pomacentridae)

The rate of environmental niche evolution describes the capability of species to explore the available environmental space and is known to vary among species owing to lineage-specific factors. Trophic specialization is a main force driving species evolution and is responsible for classical examples of adaptive radiations in fishes. We investigate the effect of trophic specialization on the rate of environmental niche evolution in the damselfish, Pomacentridae, which is an important family of tropical reef fishes. First, phylogenetic niche conservatism is not detected in the family using a standard test of phylogenetic signal, and we demonstrate that the environmental niches of damselfishes that differ in trophic specialization are not equivalent while they still overlap at their mean values. Second, we estimate the relative rates of niche evolution on the phylogenetic tree and show the heterogeneity among rates of environmental niche evolution of the three trophic groups. We suggest that behavioural characteristics related to trophic specialization can constrain the evolution of the environmental niche and lead to conserved niches in specialist lineages. Our results show the extent of influence of several traits on the evolution of the environmental niche and shed new light on the evolution of damselfishes, which is a key lineage in current efforts to conserve biodiversity in coral reefs.     

Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other's closest living relatives

Many filamentous cyanobacteria reduce atmospheric nitrogen in specialized differentiated cells called heterocysts. Here we present evidence that shows that members of the unicellular non-heterocyst-differentiating genus Chroococcidiopsis and the filamentous heterocyst-differentiating cyanobacteria are each other's closest living relatives. Distance, maximum-parsimony, and maximum-likelihood analyses of complete small subunit ribosomal RNA gene sequences yielded highly congruent support for the monophyly of Chroococcidiopsis and the heterocyst-differentiating cyanobacteria. Our results demonstrate that the order Pleurocapsales, which traditionally contains Chroococcidiopsis, is a polyphyletic assemblage with the ability to reproduce by multiple fission having arisen independently at least twice during the cyanobacterial radiation. Our data also reject Myxosarcina as a sister taxon to Chroococcidiopsis, indicating that the numerous presumed shared derived characters thought to unite the two genera evolved independently. The sequence divergence within the Chroococcidiopsis lineage is comparable to and probably exceeds that in the entire heterocyst-differentiating lineage. Chroococcidiopsis forms unique survival cells under nitrogen-limiting conditions, and the sister group relationship with the heterocystous cyanobacteria shown here suggests that differentiation of these cells and heterocysts may be related processes.     

An immunological analysis of the phylogenetic relationships between two enigmatic frogs, Myobatrachus and Arenophryne

The monotypic Australian frog genera Myobatrachus and Arenophryne occur in Western Australia. Myobatrachus has a bizarre appearance with a small, narrow head and extremely short limbs—features which may represent adaptations to its forward burrowing habit and dietary specialization on termites. Because of its unusual morphology, Myobatrachus has been interpreted as a representative of an old lineage dating back to the early Tertiary or late Mesozoic era. Phylogenetic analysis of albumin evolution in these two genera, as well as five additional purportedly related frog genera, demonstrates that Myobatrachus and Arenophryne are one another's closest genetic relatives and these lineages most likely diverged in the Miocene. The genera Metacrinia and Pseudophryne are most closely related to the lineage giving rise to Myobatrachus and Arenophryne , with these two major lineages diverging in the early Miocene.     

Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas

Lake Tanganyika, the oldest of the East African Great Lakes, harbors the ecologically, morphologically, and behaviorally most complex of all assemblages of cichlid fishes, consisting of about 200 described species. The evolutionary old age of the cichlid assemblage, its extreme degree of morphological differentiation, the lack of species with intermediate morphologies, and the rapidity of lineage formation have made evolutionary reconstruction difficult. The number and origin of seeding lineages, particularly the possible contribution of riverine haplochromine cichlids to endemic lacustrine lineages, remains unclear. Our phylogenetic analyses, based on mitochondrial DNA sequences of three gene segments of 49 species (25% of all described species, up to 2,400 bp each), yield robust phylogenies that provide new insights into the Lake Tanganyika adaptive radiation as well as into the origin of the Central- and East-African haplochromine faunas. Our data suggest that eight ancient African lineages may have seeded the Tanganyikan cichlid radiation. One of these seeding lineages, probably comprising substrate spawning Lamprologus-like species, diversified into six lineages that evolved mouthbrooding during the initial stage of the radiation. All analyzed haplochromines from surrounding rivers and lakes seem to have evolved within the radiating Tanganyikan lineages. Thus, our findings contradict the current hypothesis that ancestral riverine haplochromines colonized Lake Tanganyika to give rise to at least part of its spectacular endemic cichlid species assemblage. Instead, the early phases of the Tanganyikan radiation affected Central and East African rivers and lakes. The haplochromines may have evolved in the Tanganyikan basin before the lake became a hydrologically and ecologically closed system and then secondarily colonized surrounding rivers. Apparently, therefore, the current diversity of Central and East African haplochromines represents a relatively young and polyphyletic fauna that evolved from or in parallel to lineages now endemic to Lake Tanganyika.