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Conspecific and interspecific interactions between the FEM-2 and the FEM-3 sex-determining proteins despite rapid sequence divergence.

Using degenerate oligonucleotide primers, we isolated the Caenorhabditis remanei orthologue of the C. elegans sex-determining phosphatase gene fem-2 as well as two other protein phosphatase homologues. Despite the significant sequence divergence between C. elegans and C. remanei FEM-2, we used RNAi-mediated gene knockdown to demonstrate that at least some aspects of male development require FEM-2 function in C. remanei. Consistent with this functional conservation, the conspecific interaction between the FEM-2 and the FEM-3 proteins observed in C. elegans also occurs in C. remanei. To further explore whether the rapid evolution of FEM-2 and FEM-3 affects their molecular interactions, we tested for cross-species interactions between the proteins from C. elegans, C. briggsae, and C. remanei. Although all FEM-2/FEM-3 pairs from a single species interact, only two out of six interspecific pairs bind each other, showing that FEM-2 and FEM-3 are coevolving. Both interspecific interactions involved C. briggsae FEM-3. We constructed chimeric versions of FEM-2 consisting of various combinations of the C. elegans and C. remanei proteins. C. briggsae FEM-3 interacted with all the chimeras, even those that did not interact with either C. elegans or C. remanei FEM-3. We hypothesize that the promiscuity of C. briggsae FEM-3 reflects an increased reliance on evolutionarily constrained regions of FEM-2 for binding. If so, our data support the notion that the coevolution of two interacting proteins sometimes involves a shift in the domains that contribute to binding.

Amino Acid Sequence↗

Molecular evolution of cytochrome c oxidase in high-performance fish (teleostei: Scombroidei).

The 13 peptides encoded by vertebrate mitochondrial DNA (mtDNA) are essential subunits of oxidative phosphorylation (OXPHOS) enzymes. These genes normally experience purifying selection and also coevolve with nuclear-encoded subunits of OXPHOS complexes. However, the role of positive selection on mtDNA evolution is still unclear, as most examples of intergenomic coevolution appear to be the result of compensation by nuclear-encoded genes for mildly deleterious mtDNA mutations, and not simultaneous positive selection in both genomes. Organisms that have experienced strong selective pressures to increase aerobic capacity or adapt to changes in thermal environment may be better candidates in which to examine the impact of positively selected changes on mtDNA evolution. The tuna (suborder Scombroidei, family Scombridae) and billfish (suborder Scombroidei, families Xiphiidae and Istiophoridae) are highly aerobic fish with multiple specializations in muscle energetics, including a high mitochondrial content and regional endothermy. We examined the role of positively selected mtDNA substitutions in the production of these unique phenotypes. Focusing on a catalytic subunit of cytochrome c oxidase (COX II), we found that the rate ratio of nonsynonymous (d(N); amino acid changing)-to-synonymous (d(S); silent) substitutions was not increased in lineages leading to the tuna but was significantly increased in the lineage preceding the billfish. Furthermore, there are a number of individual positively selected sites that, when mapped onto the COX crystal structure, appear to interact with other COX subunits and may affect OXPHOS function and regulation in billfish.

Animals↗

Evolution of +1 programmed frameshifting signals and frameshift-regulating tRNAs in the order Saccharomycetales.

Programmed translational frameshifting is a ubiquitous but rare mechanism of gene expression in which mRNA sequences cause the translational machinery to shift reading frames with extreme efficiency, up to at least 50%. The mRNA sequences responsible are deceptively simple; the sequence CUU-AGG-C causes about 40% frameshifting when inserted into an mRNA in the yeast Saccharomyces cerevisiae. The high efficiency of this site depends on a set of S. cerevisiae tRNA isoacceptors that perturb the mechanism of translation to cause the programmed translational error. The simplicity of the system might suggest that it could evolve frequently and perhaps be lost as easily. We have investigated the history of programmed +1 frameshifting in fungi. We find that frameshifting has persisted in two structural genes in budding yeasts, ABP140 and EST3 for about 150 million years. Further, the tRNAs that stimulate the event are equally old. Species that diverged from the lineage earlier both do not employ frameshifting and have a different complement of tRNAs predicted to be inimical to frameshifting. The stability of the coevolution of protein coding genes and tRNAs suggests that frameshifting has been selected for during the divergence of these species.

Amino Acid Sequence↗

Contrasting evolutionary patterns in Drosophila immune receptors.

Vertebrate immune system molecules that bind directly to parasites are commonly subject to strong directional natural selection, probably because they are engaged in an evolutionary arms race with parasites. We have investigated whether similar patterns of evolution are seen in components of the Drosophila immune system that bind parasite-derived molecules. In insects, TEPs (thioester-containing proteins) function as opsonins, binding to parasites and promoting their phagocytosis or encapsulation. The Drosophila melanogaster genome encodes four TEPs, three of which are upregulated after an immune challenge. We report that two of these three Drosophila genes evolve rapidly under positive selection and that, in both TepI and TepII, the "bait-like region" (also known as the variable region) shows the strongest signature of positive selection. This region may be the site of proteolytic cleavage that leads to the activation of the molecule. It is possible that the proteolytic activation of TEPs is a target of host-parasite coevolution, with parasites evolving to prevent proteolysis, which in turn favors mutations in the bait-like region that restore the response. We also sequenced three gram-negative binding proteins (GNBPs) and two immune-induced peptides with strong homology to the GNBPs. In contrast to the Tep genes, the GNBP genes are highly conserved. We discuss the reasons why different components of the immune system have such different patterns of evolution.

Animals↗

Molecular phylogeny, evolution, and functional divergence of the LSD1-like gene family: inference from the rice genome.

The identification of LSD1-like genes in parasite, green algae, moss, pine, and monocot and dicot species allowed us to trace the phylogenetic history of this gene family. Computational analysis showed that the diversification of members of this family could be dated back to the early stage of plant evolution. The evolution of plant LSD1-like genes was possibly shaped by two duplication events. These proteins, which contain three copies of the LSD1 zinc finger (zf-LSD1) domain within their entire polypeptides and play crucial roles in modulating disease defense and cell death, resulted from the second duplication. A gain of zf-LSD1 domain model was reasonable for explaining the origination of three-zf-LSD1 domain-containing proteins. The zf-LSD1 domain phylogeny showed that the middle (M) and C-terminal (C) domains originated from a common ancestor; the N-terminal (N) domain might be more ancient than the former two. The divergence of the N, M, and C domains was well before the monocot-dicot split. Coevolution analysis revealed that four intramolecular domain pairs, including the N domain and the interregion between the M and the C domains (INTER2), the M and C domain, the N- and C-terminus, and the M domain and C-terminus, possibly coevolved during the evolution of three-zf-LSD1 domain-containing proteins. The three zf-LSD1 domains are evolutionary conserved. Thus, the differences at the N- and C-terminus would be crucial for functional specificity of LSD1 genes. Strong functional constraints should work on the zf-LSD1 domains, whereas reduced functional constraint was found in the INTER2 region. Functional divergence analysis showed that three-zf-LSD1 domain-containing proteins were significantly functionally divergent from those proteins containing only one zf-LSD1 domain, a result demonstrating that shifted evolutionary rates between the two clusters were significantly different from each other.

Amino Acid Sequence↗

Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus?

In the theory of viral eukaryogenesis I propose here, the eukaryotic nucleus evolved from a complex DNA virus. It is proposed that the virus established a persistent presence in the cytoplasm of a methanogenic mycoplasma and evolved into the eukaryotic nucleus by acquiring a set of essential genes from the host genome and eventually usurping its role. It is proposed that several characteristic features of the eukaryotic nucleus derive from its viral ancestry. These include mRNA capping, linear chromosomes, and separation of transcription from translation. In the model, phagocytosis and other membrane fusion-based processes are derived from viral membrane fusion processes and evolved in concert with the nucleus. The coevolution of phagocytosis and the nucleus rendered much of the host archaeal genome redundant since the protoeukaryote could obtain raw materials and energy by engulfing bacterial syntrophs/prey. This redundancy allowed loss of the archaeal chromosome, generating an organism with eukaryotic features. The evolution of phagocytosis allowed the eukaryotes to be the first organisms to occupy the niche of predator.

Amino Acid Sequence↗

On the evolution of redundancy in genetic codes.

We simulate a deterministic population genetic model for the coevolution of genetic codes and protein-coding genes. We use very simple assumptions about translation, mutation, and protein fitness to calculate mutation-selection equilibria of codon frequencies and fitness in a large asexual population with a given genetic code. We then compute the fitnesses of altered genetic codes that compete to invade the population by translating its genes with higher fitness. Codes and genes coevolve in a succession of stages, alternating between genetic equilibration and code invasion, from an initial wholly ambiguous coding state to a diversified frozen coding state. Our simulations almost always resulted in partially redundant frozen genetic codes. Also, the range of simulated physicochemical properties among encoded amino acids in frozen codes was always less than maximal. These results did not require the assumption of historical constraints on the number and type of amino acids available to codes nor on the complexity of proteins, stereochemical constraints on the translational apparatus, nor mechanistic constraints on genetic code change. Both the extent and timing of amino-acid diversification in genetic codes were strongly affected by the message mutation rate and strength of missense selection. Our results suggest that various omnipresent phenomena that distribute codons over sites with different selective requirements--such as the persistence of nonsynonymous mutations at equilibrium, the positive selection of the same codon in different types of sites, and translational ambiguity--predispose the evolution of redundancy and of reduced amino acid diversity in genetic codes.

Codon↗

Obcells as proto-organisms: membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis.

I attempt to sketch a unified picture of the origin of living organisms in their genetic, bioenergetic, and structural aspects. Only selection at a higher level than for individual selfish genes could power the cooperative macromolecular coevolution required for evolving the genetic code. The protein synthesis machinery is too complex to have evolved before membranes. Therefore a symbiosis of membranes, replicators, and catalysts probably mediated the origin of the code and the transition from a nucleic acid world of independent molecular replicators to a nucleic acid/protein/lipid world of reproducing organisms. Membranes initially functioned as supramolecular structures to which different replicators attached and were selected as a higher-level reproductive unit: the proto-organism. I discuss the roles of stereochemistry, gene divergence, codon capture, and selection in the code's origin. I argue that proteins were primarily structural not enzymatic and that the first biological membranes consisted of amphipathic peptidyl-tRNAs and prebiotic mixed lipids. The peptidyl-tRNAs functioned as genetically-specified lipid analogues with hydrophobic tails (ancestral signal peptides) and hydrophilic polynucleotide heads. Protoribosomes arose from two cooperating RNAs: peptidyl transferase (large subunit) and mRNA-binder (small subunit). Early proteins had a second key role: coupling energy flow to the phosphorylation of gene and peptide precursors, probably by lithophosphorylation by membrane-anchored kinases scavenging geothermal polyphosphate stocks. These key evolutionary steps probably occurred on the outer surface of an 'inside out-cell' or obcell, which evolved an unambiguous hydrophobic code with four prebiotic amino acids and proline, and initiation by isoleucine anticodon CAU; early proteins and nucleozymes were all membrane-attached. To improve replication, translation, and lithophosphorylation, hydrophilic substrate-binding and catalytic domains were later added to signal peptides, yielding a ten-acid doublet code. A primitive proto-ecology of molecular scavenging, parasitism, and predation evolved among obcells. I propose a new theory for the origin of the first cell: fusion of two cup-shaped obcells, or hemicells, to make a protocell with double envelope, internal genome and ribosomes, protocytosol, and periplasm. Only then did water-soluble enzymes, amino acid biosynthesis, and intermediary metabolism evolve in a concentrated autocatalytic internal cytosolic soup, causing 12 new amino acid assignments, termination, and rapid freezing of the 22-acid code. Anticodons were recruited sequentially: GNN, CNN, INN, and *UNN. CO2 fixation, photoreduction, and lipid synthesis probably evolved in the protocell before photophosphorylation. Signal recognition particles, chaperones, compartmented proteases, and peptidoglycan arose prior to the last common ancestor of life, a complex autotrophic, anaerobic green bacterium.

Anticodon↗

The CD45 locus in cattle: allelic polymorphism and evidence for exceptional positive natural selection.

Cattle in Africa are a genetically diverse population that has resulted from successive introduction of Asian Bos indicus and European B. taurus cattle. However, analysis of mitochondrial genetic diversity in African cattle identified three lineages, one associated with Asian B. indicus, one with European B. taurus, and a third ascribed to an indigenous African sub-species of cattle. Due to their extended coevolution, indigenous African herbivores are generally tolerant to endemic African pathogens. We are interested in identifying alleles derived from the indigenous African cattle that may be associated with tolerance to African pathogens. An analysis of the locus which encodes the abundant plasma membrane-associated tyrosine phosphatase, CD45, identified three highly divergent allelic families in Kenya Boran cattle. Analysis of allelic distribution in a diverse range of cattle populations suggests a European B. taurus, an Asian B. indicus, and an African origin. This demonstrates not only significant allelic polymorphism at the CD45 locus in cattle but also convincing autosomal evidence for a distinct African sub-species of cattle. Furthermore, maximum-likelihood analysis of selection pressures revealed that the CD45 locus is subject to exceptionally strong natural selection which we suggest may be pathogen driven.

Africa↗

TNFB polymorphisms characterize three lineages of TNF region microsatellite haplotypes.

The human major histocompatibility complex (MHC) contains a variety of genes, many of which are highly polymorphic and of immunological importance. A database of MHC extended haplotypes was used to integrate experimental, cell line, and population data. Three alleles of the human TNF-beta (lymphotoxin-alpha) gene were identified, named TNFB*1SL, TNFB*2LL, and TNFB*1LS, each representing a different lineage in the evolution of TNF region haplotypes. Lower variability in the length of the associated microsatellite alleles indicates that *1SL characterizes the youngest of the three haplotype lineages. Microsatellite haplotypes in the two older lineages show evidence for a coevolution of alleles through concerted expansions. Genetic predispositions to high and low TNF-alpha (cachectin) responses seem to have evolved independently in more than one lineage. The literature data suggest different, or even opposite, associations concerning the regulation of TNF-alpha in macrophages and lymphoid cells. Microsatellite ud may be the most informative marker for studies of the associations of individual TNF region markers with secretion levels, immunity, and disease.

Alleles↗

Floodplain Formation and Cottonwood Colonization Patterns on the Willamette River, Oregon, USA.

/ Using a series of aerial photographs taken between 1936 and 1996, we trace coevolution of floodplain and riparian forest on the Willamette River. Within-channel barforms appear to be the predominant incipient floodplain landform and habitat for primary succession. Interlinked development of bar(s) and erosion of near banks, filling of channels, and establishment and growth of cottonwoods and willows results in coalescence with older floodplain. Sizeand internal structure of riparian forest patches reflect evolution of underlying barforms or channel beds. Floodplain matures as the active channel migrates away by repetition of the bar formation and near-bank erosion process, or is progressively abandoned by infilling and/or constriction with a bar. Other parts of the floodplain are recycled as eroding banks provide the coarse sediment and large woody debris for building new bars. A multichannel planform is maintained as building bars split flow; channels lengthen as bars and islands join into larger assemblages. Avulsion appears to cut new channels only short distances. Given the central role of bars and islands in building new floodplain habitat, we identify their area as a geomorphic indicator of river-floodplain integrity. We measure an 80% decline in bar and island area between 1910 and 1988 within a 22-km section. Dams, riprap, logging, and gravel mining may all be contributing to diminished bar formation rates. Removing obstacles to natural riparian forest creation mechanisms is necessary to regenerate the river-floodplain system and realize its productive potential.

Journal Article↗

The impact of the thermal sensitivity of cytochrome c oxidase on the respiration rate of Arctic charr red muscle mitochondria. pierre_blier@uqar.qc.ca.

To assess if cytochrome c oxidase could determine the response of mitochondrial respiration to changes in environmental temperature in ectotherms, we performed KCN titration of the respiration rate and cytochrome c oxidase activity in mitochondria from Arctic charr (Salvelinusfontinalis) muscle at four different temperatures (1 degrees C, 6 degrees C, 12 degrees C, and 18 degrees C). Our data showed an excess of cytochrome c oxidase activity over the mitochondrial state 3 respiration rate. Mitochondrial oxygen consumption rates reached approximately 12% of the cytochrome c oxidase maximal capacity at every temperature. Also, following titration, the mitochondrial respiration rate significantly decreased when KCN reached concentrations that inhibit almost 90% of the cytochrome c oxidase activity. This strongly supports the idea that the thermal sensitivity of the maximal mitochondrial respiration rate cannot be dictated by the effect of temperature on cytochrome c oxidase catalytic capacity. Furthermore, the strong similarity of the Q10s of mitochondrial respiration and cytochrome c oxidase activity suggests a functional or structural link between the two. The functional link could be coevolution of parts of the mitochondrial system to maintain optimal functions in most of the temperature range encountered by organisms.

Animals↗

Non-LTR retrotransposons with unique integration preferences downstream of Dictyostelium discoideum tRNA genes.

Retrotransposable elements are genetic enti ties which move and replicate within host cell genomes We have previously reported on the structures and ge nomic distributions of two non-long terminal repea (non-LTR) retrotransposons, DRE and Tdd-3, in the eukaryotic microorganism Dictyostelium discoideum DRE elements are found inserted upstream, and Tdd-3 elements downstream, of transfer RNA (tRNA) genes with remarkable position and orientation specificities The data set currently available from the Dictyostelium Genome Project led to the characterisation of two repetitive DNA elements which are related to the D. discoideum non-LTR retrotransposon Tdd-3 in both their structural properties and genomic distributions. It appears from our data that in the D. discoideum genome tRNA genes are major targets for the insertion of mobilised non-LTR retrotransposons. This may be interpreted as the consequence of a process of coevolution, allowing a viable population of retroelements to transpose without being deleterious to the small microbial host genome which carries only short intergenic DNA sequences. A new nomenclature is introduced to designate all tRNA gene-targeted non-LTR retrotransposons (TREs) in the D. discoideum genome. TREs inserted 5' and 3' of tRNA genes are named TRE5 and TRE3, respectively. According to this nomenclature DRE and Tdd-3 are renamed TRE5-A and TRE3-A, respectively. The new retroelements described in this study are named TRE3-B (formerly RED) and TRE3-C.

Amino Acid Sequence↗

Toward an ecological synthesis: a case for habitat selection.

Habitat selection, and its associated density and frequency-dependent evolution, has a profound influence on such vital phenomena as population regulation, species interactions, the assembly of ecological communities, and the origin and maintenance of biodiversity. Different strategies of habitat selection, and their importance in ecology and evolution, can often be revealed simply by plots of density in adjacent habitats. For individual species, the strategies are closely intertwined with mechanisms of population regulation, and with the persistence of populations through time. For interacting species, strategies of habitat selection are not only responsible for species coexistence, but provide one of the most convenient mechanisms for measuring competition, and the various community structures caused by competitive interactions. Other kinds of interactions, such as those between predators and prey, demonstrate that an understanding of the coevolution of habitat-selection strategies among strongly interacting species is essential to properly interpret their spatial and temporal dynamics. At the evolutionary scale, the frequency dependence associated with habitat selection may often allow populations to diverge and diversify into separate species. Habitat selection thereby demonstrates how we can map microevolutionary strategies in behavior onto their population and community consequences, and from there, onto macroevolutionary patterns of speciation and adaptive radiation. We can anticipate that future studies of habitat selection will not only help us complete those maps, but that they will also continue to enrich the panoply of ideas that shape evolutionary ecology.

Animals↗

Gender- and sequence-dependent predation within group colonizers of defended plants: a constraint on cheating among bark beetles?

Bark beetles engage in one of the most pronounced examples of group procurement of defended plants. Their aggregation pheromones attract both sexes and are essential to overcome constitutive and rapidly inducible lethal defenses. The relative benefits to senders versus receivers of these signals are only partly understood. Because the initial stage of host entry can be hazardous, there may be benefit to a cheating strategy, whose practitioners respond to pheromones but do not engage in host searching. Several disadvantages to cheating have been proposed, but the role of predators has not been considered. Predators exploit bark beetle pheromones to locate prey, accumulate at the breeding site, and consume adult bark beetles before they enter the tree. Preliminary experiments quantified arrival patterns in the field. We used a laboratory assay to investigate relative predation on pioneers (those that initially select and enter hosts) and responders (those that arrive at a host in response to pheromones) during host colonization. Our model system utilized the pine engraver, Ips pini, which exhibits male harem polygamy. We allowed male I. pini to colonize host tissue and added females 1 day later. Also 1 day later, we variably added additional males and predacious checkered beetles, Thanasimus dubius. These treatments included two densities of males and three densities of predators that were selected to emulate field conditions. Responding males experienced higher predation than pioneers. T. dubius ate more males than females, independent of the presence or absence of responding males. T. dubius affected the distribution of females per male, although the number of females that survived to construct ovipositional galleries was constant. We discuss the viability of cheating, implications for biological control, and predator-prey coevolution in this cooperative, group-colonizing herbivore.

Adaptation, Physiological↗

Causal mechanisms underlying host specificity in bat ectoparasites.

In parasites, host specificity may result either from restricted dispersal capacity or from fixed coevolutionary host-parasite adaptations. Knowledge of those proximal mechanisms leading to particular host specificity is fundamental to understand host-parasite interactions and potential coevolution of parasites and hosts. The relative importance of these two mechanisms was quantified through infection and cross-infection experiments using mites and bats as a model. Monospecific pools of parasitic mites (Spinturnix myoti and S. andegavinus) were subjected either to individual bats belonging to their traditional, native bat host species, or to another substitute host species within the same bat genus (Myotis). The two parasite species reacted differently to these treatments. S. myoti exhibited a clear preference for, and had a higher fitness on, its native host, Myotis myotis. In contrast, S. andegavinus showed no host choice, although its fitness was higher on its native host M. daubentoni. The causal mechanisms mediating host specificity can apparently differ within closely related host-parasite systems.

Animals↗

Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs?

Plants are often attacked by multiple enemies, including pathogens and herbivores. While many plant secondary metabolites show specific effects toward either pathogens or herbivores, some can affect the performance of both these groups of natural enemies and are considered to be "generalized defense compounds". We tested whether aucubin and catalpol, two iridoid glycosides present in ribwort plantain (Plantago lanceolata), confer in vivo resistance to both the generalist insect herbivore Spodoptera exigua and the biotrophic fungal pathogen Diaporthe adunca using plants from P. lanceolata lines that had been selected for high- and low-leaf iridoid glycoside concentrations for four generations. The lines differed approximately three-fold in the levels of these compounds. Plants from the high-selection line showed enhanced resistance to both S. exigua and D. adunca, as evidenced by a smaller lesion size and a lower fungal growth rate and spore production, and a lower larval growth rate and herbivory under both choice and no-choice conditions. Gravimetric analysis revealed that the iridoid glycosides acted as feeding deterrents to S. exigua, thereby reducing its food intake rate, rather than having post-ingestive toxic effects as predicted from in vitro effects of hydrolysis products. We suggest that the bitter taste of iridoid glycosides deters feeding by S. exigua, whereas the hydrolysis products formed after tissue damage following fungal infection mediate pathogen resistance. We conclude that iridoid glycosides in P. lanceolata can serve as broad-spectrum defenses and that selection for pathogen resistance could potentially result in increased resistance to generalist insect herbivores and vice versa, resulting in diffuse rather than pairwise coevolution.

Adaptation, Physiological↗

Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts.

Antagonistic host-parasite interactions lead to coevolution of host defenses and parasite virulence. Such adaptation by parasites to host defenses may occur to the detriment of the ability of parasites to exploit alternative hosts, causing parasite specialization and speciation. We investigated the relationship between level of anti-parasite defense in hosts and taxonomic richness of two chewing louse suborders (Phthiraptera: Amblycera, Ischnocera) on birds. While Amblyceran lice tend to occur in contact with host skin, feed on host skin and chew emerging tips of developing feathers to obtain blood, Ischnoceran lice live on feathers and feed on the non-living keratin of feather barbules. We hypothesized that Amblyceran abundance and richness would have evolved in response to interaction with the immune system of the host, while Ischnoceran taxonomic richness would have evolved independently of immunological constraints. In an interspecific comparison, the abundance of Ischnocerans was positively related to host body size, while host body mass and Ischnoceran taxonomic richness accounted for the abundance of Amblycerans. Amblyceran taxonomic richness was predicted by the intensity of T-cell mediated immune response of nestling hosts, while the T-cell response of adults had no significant effect. In contrast, Ischnoceran taxonomic richness was not predicted by host T-cell responses. These results suggest that the taxonomic richness of different parasite taxa is influenced by different host defenses, and they are consistent with the hypothesis that increasing host allocation to immune defense increases Amblyceran biodiversity.

Animals↗