Host ecology and life-history traits associated with blood parasite species richness in birds

Identifying host traits associated with the number of different parasite species or strains harboured by a particular host species can have important implications for understanding the impact of parasitism on hosts. We investigated associations between host ecology and life history, and parasite richness and prevalence of the four major avian blood parasite genera. We used an extensive data on blood parasite infections and host ecology in 263 bird species from the Western Palearctic, combining species-specific data with a comparative approach to control for similarity in phenotype among host species due to the effects of common phylogenetic descent. Adult survival rate negatively correlated with the number of parasite species infecting a host species when controlling for similarity due to common descent and body mass. In addition, the prevalence of Haemoproteus, Plasmodium and Leucocytozoon was higher in species harbouring a richer parasite assemblage. These results suggest that the impact on host fitness caused by avian haematozoa may be underestimated in natural populations if the exacerbated virulence associated with exposure to multiple parasites is not taken into account.     

Coevolution between parasite virulence and host life-history traits

Epidemiological models generally explore the evolution of parasite life-history traits, namely, virulence and transmission, against a background of constant host life-history traits. However, life-history models have predicted the evolution of host traits in response to parasitism. The coevolution of host and parasite life-history traits remains largely unexplored. We present an epidemiological model, based on resource allocation theory, that provides an analysis of the coevolution between host reproductive effort and parasite virulence. This model allows for hosts with either a fixed (i.e., genetic) or conditional (i.e., a phenotypically plastic) response to parasitism. It also considers superinfections. We show that parasitism always favors increased allocation to host reproduction, but because of epidemiological feedbacks, the evolutionarily stable host reproductive effort does not always increase with parasite virulence. Superinfection drives the evolution of parasite virulence and acts on the evolution of the host through parasite evolution, generally leading to higher host reproductive effort. Coevolution, as opposed to cases where only one of the antagonists evolves, may generate correlations between host and parasite life-history traits across environmental gradients affecting the fecundity or the survival of the host. Our results provide a theoretical framework against which experimental coevolution outcomes or field observations can be contrasted.     

Symbiont modifies host life-history traits that affect gene flow

The evolution of herbivore-host plant specialization requires low levels of gene flow between populations on alternate plant species. Accordingly, selection for host plant specialization is most effective when genotypes have minimal exposure to, and few mating opportunities with individuals from, alternate habitats. Maternally transmitted bacterial symbionts are common in insect herbivores and can influence host fecundity under a variety of conditions. Symbiont-mediated effects on host life-history strategies, however, are largely unknown. Here, we show that the facultative bacterial symbiont Candidatus Regiella insecticola strikingly alters both dispersal and mating in the pea aphid, Acyrthosiphon pisum. Pea aphids containing Regiella produced only half the number of winged offspring in response to crowding and, for two out of three aphid lineages, altered the timing of sexual reproduction in response to conditions mimicking seasonal changes, than did aphids lacking Regiella. These symbiont-associated changes in dispersal and mating are likely to have played a key role in the initiation of genetic differentiation and in the evolution of pea aphid-host plant specialization. As symbionts are widespread in insects, symbiont-induced life history changes may have promoted specialization, and potentially speciation, in many organisms.     

Contrasting life-history traits of two sympatric smooth-hound species: implication for vulnerability

In this study, life-history traits (maximum and average size, size at maturity and fecundity) of two congeneric smooth-hounds, Mustelus mustelus and Mustelus punctulatus, which share a geographical distribution and experience a similar fishing exploitation, were estimated and compared between species. The results indicated a lower maximum and average size, a lower size at maturity and a higher fecundity in M. punctulatus compared with those in M. mustelus. Considering that these two species co-occur in the same areas and are caught by the same fishing gears, the results indicate a higher vulnerability to exploitation of M. mustelus compared with that of M. punctulatus.     

Rebuilding community ecology from functional traits

There is considerable debate about whether community ecology will ever produce general principles. We suggest here that this can be achieved but that community ecology has lost its way by focusing on pairwise species interactions independent of the environment. We assert that community ecology should return to an emphasis on four themes that are tied together by a two-step process: how the fundamental niche is governed by functional traits within the context of abiotic environmental gradients; and how the interaction between traits and fundamental niches maps onto the realized niche in the context of a biotic interaction milieu. We suggest this approach can create a more quantitative and predictive science that can more readily address issues of global change.     

Spatial ecology of multiple parasitoids of a patchily‐distributed host: implications for species coexistence

1. The coexistence of multiple species sharing similar but spatially fragmented resources (e.g. parasitoids sharing a host species) may depend on their relative competitive and dispersal abilities, or on fine‐scale resource partitioning. Four generalist and one specialist parasitoid species associated with the holly leaf miner, Phytomyza ilicis, in a woodland network of 127 holly trees were investigated. 2. To understand coexistence and persistence of these potential competitors, patterns of occurrence in relation to patch size and isolation, vertical stratum within patches, and incidence and abundance of potential competitors were documented. Field experiments creating empty habitat patches suggested that dispersal rather than local demographic processes determines abundance and incidence. 3. Parasitoids showed species‐specific responses to patch properties, with the incidence of species determined mostly by patch size. Parasitism rates were less clearly related to patch characteristics, but parasitism rates for most species were lower in patches where the numerically dominant parasitoid species, Chrysocharis gemma, was present. No evidence of vertical stratification was found in species composition or abundance within patches, making it unlikely that coexistence is enhanced by fine‐scale resource division. 4. Overall, the patterns detected may be attributed to the distribution of C. gemma and differences in species' ecology other than dispersal ability. The life history of C. gemma may allow it to pre‐emptively exploit a large fraction of the available hosts, avoiding direct competition with other parasitoids. In contrast, direct competition is more likely among the pupal parasitoids Cyrtogaster vulgaris, Chrysocharis pubicornis, and Sphegigaster flavicornis which have a similar biology and phenology. For these species, coexistence may be facilitated by contrasting incidence in relation to patch size and isolation.     

Local adaptation in brown trout early life-history traits: implications for climate change adaptability

Knowledge of local adaptation and adaptive potential of natural populations is becoming increasingly relevant due to anthropogenic changes in the environment, such as climate change. The concern is that populations will be negatively affected by increasing temperatures without the capacity to adapt. Temperature-related adaptability in traits related to phenology and early life history are expected to be particularly important in salmonid fishes. We focused on the latter and investigated whether four populations of brown trout (Salmo trutta) are locally adapted in early life-history traits. These populations spawn in rivers that experience different temperature conditions during the time of incubation of eggs and embryos. They were reared in a common-garden experiment at three different temperatures. Quantitative genetic differentiation (QST) exceeded neutral molecular differentiation (FST) for two traits, indicating local adaptation. A temperature effect was observed for three traits. However, this effect varied among populations due to locally adapted reaction norms, corresponding to the temperature regimes experienced by the populations in their native environments. Additive genetic variance and heritable variation in phenotypic plasticity suggest that although increasing temperatures are likely to affect some populations negatively, they may have the potential to adapt to changing temperature regimes.     

Evolution of host life-history traits in a spatially structured host-parasite system

Most models for the evolution of host defense against parasites assume that host populations are not spatially structured. Yet local interactions and limited dispersal can strongly affect the evolutionary outcome, because they significantly alter epidemiological feedbacks and the spatial genetic structuring of the host and pathogen populations. We provide a general framework to study the evolution of a number of host life-history traits in a spatially structured host population infected by a horizontally transmitted parasite. Our analysis teases apart the selective pressures on hosts and helps disentangle the direct fitness effect of mutations and their indirect effects via the influence of spatial structure on the genetic, demographic, and epidemiological structure of the host population. We then illustrate the evolutionary consequences of spatial structure by focusing on the evolution of two host defense strategies against parasitism: suicide upon infection and reduced transmission. Because they bring no direct fitness benefit, these strategies are counterselected or selectively neutral in a nonspatial setting, but we show that they can be selected for in a spatially structured environment. Our study thus sheds light on the evolution of altruistic defense mechanisms that have been observed in various biological systems.     

Adaptive genetic diversity of dominant species contributes to species co-existence and community assembly

The synthesis of evolutionary biology and community ecology aims to understand how genetic variation within one species can shape community properties and how the ecological properties of a community can drive the evolution of a species. A rarely explored aspect is whether the interaction of genetic variation and community properties depends on the species'' ecological role. Here we investigated the interactions among environmental factors, species diversity, and the within-species genetic diversity of species with different ecological roles. Using high-throughput DNA sequencing, we genotyped a canopy-dominant tree species, Parashorea chinensis, and an understory-abundant species, Pittosporopsis kerrii, from fifteen plots in Xishuangbanna tropical seasonal rainforest and estimated their adaptive, neutral and total genetic diversity; we also surveyed species diversity and assayed key soil nutrients. Structural equation modelling revealed that soil nitrogen availability created an opposing effect in species diversity and adaptive genetic diversity of the canopy-dominant Pa. chinensis. The increased adaptive genetic diversity of Pa. chinensis led to greater species diversity by promoting co-existence. Increased species diversity reduced the adaptive genetic diversity of the dominant understory species, Pi. kerrii, which was promoted by the adaptive genetic diversity of the canopy-dominant Pa. chinensis. However, such relationships were absent when neutral genetic diversity or total genetic diversity were used in the model. Our results demonstrated the important ecological interaction between adaptive genetic diversity and species diversity, but the pattern of the interaction depends on the identity of the species. Our results highlight the significant ecological role of dominant species in competitive interactions and regulation of community structure.     

Genetic variation and covariation of aphid life-history traits across unrelated host plants

A central paradigm of life-history theory is the existence of resource mediated trade-offs among different traits that contribute to fitness, yet observations inconsistent with this tenet are not uncommon. We previously found a clonal population of the aphid Myzus persicae to exhibit positive genetic correlations among major components of fitness, resulting in strong heritable fitness differences on a common host. This raises the question of how this genetic variation is maintained. One hypothesis states that variation for resource acquisition on different hosts may override variation for allocation, predicting strong fitness differences within hosts as a rule, but changes in fitness hierarchies across hosts due to trade-offs. Therefore, we carried out a life-table experiment with 17 clones of M. persicae, reared on three unrelated host plants: radish, common lambsquarters and black nightshade. We estimated the broad-sense heritabilities of six life-history traits on each host, the genetic correlations among traits within hosts, and the genetic correlations among traits on different hosts (cross-environment genetic correlations). The three plants represented radically different environments with strong effects on performance of M. persicae, yet we detected little evidence for trade-offs. Fitness components were positively correlated within hosts but also between the two more benign hosts (radish and lambsquarters), as well as between those and another host tested earlier. The comparison with the most stressful host, nightshade, was hampered by low survival. Survival on nightshade also exhibited genetic variation but was unrelated to fitness on other hosts. Acknowledging that the number of environments was necessarily limited in a quantitative genetic experiment, we suggest that the rather consistent fitness hierarchies across very different plants provided little evidence to support the idea that the clonal variation for life-history traits and their covariance structure are maintained by strong genotypexenvironment interactions with respect to hosts. Alternative explanations are discussed.     

Interpopulation variation in life-history traits of Poeciliopsis prolifica: implications for the study of placental evolution

Placental reproduction is widespread across vertebrate taxa, but little is known about its life-history correlates and putative adaptive value. We studied variation in life-history traits in two populations of the placental poeciliid fish Poeciliopsis prolifica to determine whether differences in post-fertilization maternal provisioning to embryos have a genetic basis and how food availability affects reproduction. Life histories were characterized for wild-caught females and for second-generation lab-born females raised under two levels of food availability. We found that the two populations did not differ significantly in the wild for any life-history traits except for the lipid dry weight in females and in embryos at an advanced stage of development. When environmental effects were experimentally controlled, however, populations exhibited significant differences in several traits, including the degree of maternal provisioning to embryos. Food availability significantly affected female size at first parturition, brood size and offspring dry weight at birth. Altogether, these results demonstrate that population differences in maternal provisioning and other life-history traits have a genetic basis and show a plastic response to food availability. We infer that phenotypic plasticity may mask population differences in the field. In addition, when comparing life-history patterns in these two populations with known patterns in placental and non-placental poeciliids, our results support the hypotheses that placentation is an adaptive reproductive strategy under high-resource conditions but that it may represent a cost under low-food conditions. Finally, our results highlight that age at maturity and reproductive allotment may be key life-history traits accompanying placental evolution.     

Population structure in a common Caribbean coral-reef fish: implications for larval dispersal and early life-history traits

Genetic population structure throughout the Caribbean Basin for one of the most common and widespread reef fish species, the bicolour damselfish Stegastes partitus was examined using microsatellite DNA markers. Spatial autocorrelation analysis showed a significant positive correlation between genetic and geographic distance (isolation by distance) over distances <1000 km, suggesting that populations are connected genetically but probably not demographically, i.e. over shorter time scales. A difference in spatial patterns of populations in the eastern v. the western Caribbean also raises the probability of an important role for meso-scale oceanographic features and landscape complexity within the same species. A comparison of S. partitus population structure and life-history traits with those of two other species of Caribbean reef fish studied earlier showed the findings to be concordant with a common hypothesis that shorter pelagic larval dispersal periods are associated with smaller larval dispersal scales.     

Endophytic Phomopsis species: host range and implications for diversity estimates

Foliar endophyte assemblages of teak trees growing in dry deciduous and moist deciduous forests of Nilgiri Biosphere Reserve were compared. A species of Phomopsis dominated the endophyte assemblages of teak, irrespective of the location of the host trees. Internal transcribed spacer sequence analysis of 11 different Phomopsis isolates (ten from teak and one from Cassia fistula) showed that they fall into two groups, which are separated by a relatively long branch that is strongly supported. The results showed that this fungus is not host restricted and that it continues to survive as a saprotroph in teak leaf, possibly by exploiting senescent leaves as well as the litter. Although the endophyte assemblage of a teak tree growing about 500 km from the forests was also dominated by a Phomopsis sp., it separated into a different group based on internal transcribed spacer sequence analysis. Our results with an endophytic Phomopsis sp. reinforce the earlier conclusions reached by others for pathogenic Phomopsis sp., i.e., that this fungus is not host specific, and the species concept of Phomopsis needs to be redefined.     

Integrating species life-history traits and patterns of deforestation in amphibian conservation planning

Aim  To identify priority areas for amphibian conservation in southeastern Brazil, by integrating species life-history traits and patterns of deforestation.
Location  State of São Paulo, Brazil.
Methods  We used the software M arxan to evaluate different scenarios of amphibian conservation planning. Our approach differs from previous methods by explicitly including two different landscape metrics; habitat split for species with aquatic larvae, and habitat loss for species with terrestrial development. We evaluated the effect of habitat requirements by classifying species breeding habitats in five categories (flowing water, still water permanent, still water temporary, bromeliad or bamboo, and terrestrial). We performed analyses using two scales, grid cells and watersheds and also considered nature preserves as protected areas.
Results  We found contrasting patterns of deforestation between coastal and inland regions. Seventy-six grid cells and 14 watersheds are capable of representing each species at least once. When accounting for grid cells already protected in state and national parks and considering species habitat requirements we found 16 high-priority grid cells for species with one or two reproductive habitats, and only one cell representing species with four habitat requirements. Key areas for the conservation of species breeding in flowing and permanent still waters are concentrated in southern state, while those for amphibians breeding in temporary ponds are concentrated in central to eastern zones. Eastern highland zones are key areas for preserving species breeding terrestrially by direct or indirect development. Species breeding in bromeliads and bamboos are already well represented in protected areas.
Main conclusions  Our results emphasize the need to integrate information on landscape configuration and species life-history traits to produce more ecologically relevant conservation strategies.     

Bat fly species richness in Neotropical bats: correlations with host ecology and host brain

Patterns of ectoparasite species richness in mammals have been investigated in various terrestrial mammalian taxa such as primates, ungulates and carnivores. Several ecological or life traits of hosts are expected to explain much of the variability in species richness of parasites. In the present comparative analysis we investigate some determinants of parasite richness in bats, a large and understudied group of flying mammals, and their obligate blood-sucking ectoparasite, streblid bat flies (Diptera). We investigate the effects of host body size, geographical range, group size and roosting ecology on the species richness of bat flies in tropical areas of Venezuela and Peru, where both host and parasite diversities are high. We use the data from a major sampling effort on 138 bat species from nine families. We also investigate potential correlation between bat fly species richness and brain size (corrected for body size) in these tropical bats. We expect a relationship if there is a potential energetic trade-off between costly large brains and parasite-mediated impacts. We show that body size and roosting in cavities are positively correlated with bat fly species richness. No effects of bat range size and group size were observed. Our results also suggest an association between body mass-independent brain size and bat fly species richness. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Thermal reaction norms in two Coenagrion damselfly species: contrasting embryonic and larval life-history traits

1. We studied the temperature‐dependence of important life‐history traits both at the embryonic (egg hatching success, embryonic development time and hatchling size) and the larval stage (larval growth rate, larval survival and larval size after 100 days) using full‐sib families of two congeneric damselflies, Coenagrion hastulatum and Coenagrion puella, that differ in latitudinal distribution. Larvae were reared in the laboratory from the egg stage at four temperatures (12, 17, 22 and 27 °C). 2. The observed patterns of thermal plasticity in embryonic traits showed that the northern species was more successful than the southern species at lower temperatures, in line with the pattern of temperature adaptation in thermal reaction norms. 3. At the larval stage, we found no consistent pattern of latitudinal compensation. The thermal family reaction norms indicate, however, the potential for latitudinal compensation to evolve. We observed an ontogenetic shift in thermal optima for larval growth rate, with a higher optimal temperature for growth rate during the first 2 weeks of the larval stage. 4. This is the first indication of the existence of latitudinal compensation at the interspecific level in an invertebrate; it is stage‐specific, being present only in the embryonic stage. We argue that compensation in the embryonic stage may be much more likely than in the larvae and stress the importance of including more then one life‐history stage when drawing conclusions about the adaptiveness of patterns in thermal reaction norms.     

Invasiveness and comparative life-history traits of exotic and indigenous Senecio species in Australia

A comparative ecological study of closely related invasive and non-invasive species, Senecio madagascariensis and S. lautus (Asteraceae), investigated what traits might confer invasive ability in very similar species. Life-history attributes of the weed S. madagascariensis were compared to five habitat-specific subspecies of S. lautus: S. l. alpinus, S. l. dissectifolius, S. l. lanceolatus and two forms of S. l. maritimus. Field populations of each taxon were monitored to compare their population ecology. Relative rates of phenological development were compared at a single location. Seed germination was studied in a laboratory experiment. Transplant experiments were conducted in a range of S. madagascariensis and S. lautus habitats to compare performance in different environments. In monitored field populations S. madagascariensis produced seedlings and reproductive cohorts more frequently, flowered for longer periods, produced more seeds and had fewer germinable achenes in the soil compared to S. lautus taxa. S. madagascariensis achenes had higher rates of germination than S. lautus in both light and dark conditions. S. madagascariensis was found to have higher rates of survival than S. lautus taxa in a range of habitats and to be faster to flower in both transplant and standard glasshouse environments. Overall S. madagascariensis performed better than S. lautus ecotypes in terms of seedling, growth and fecundity measurements and second best for achenes. Despite relatively good performance in terms of life-history traits there is no evidence that S. madagascariensis is invading S. lautus habitats. We speculate that physiological and morphological adaptations to specialised environments are a better explanation for success of Senecio taxa/ecotypes than generalised life-history trait performance. We suggest that invasiveness is essentially unpredictable, due to habitat/plant specific interactions between invader and area of introduction. In the absence of predictive theory, quarantine authorities should use a combination of methods to assess invasive potential including a database of known weeds, performance comparisons between congeneric natives and exotics in a range of habitats at proposed point of introduction and monitoring of introduced species to determine if they spread.     

Trade-offs in community ecology: linking spatial scales and species coexistence

Trade‐offs in species performances of different ecological functions is one of the most common explanations for coexistence in communities. Despite the potential for species coexistence occurring at local or regional spatial scales, trade‐offs are typically approached at a single scale. In recent years, ecologists have increasingly provided evidence for the importance of community processes at both local and regional spatial scales. This review summarizes the theoretical predictions for the traits associated with trade‐offs under different conditions and at different spatial scales. We provide a spatial framework for understanding trade‐offs, coexistence and the supportive empirical evidence. Predictions are presented that link the patterns of diversity observed to the patterns of trade‐offs that lead to coexistence at different spatial scales. Recent evidence for the evolution of trade‐offs under different conditions is provided which explores both laboratory microcosm studies and phylogenetic tests. Examining trade‐offs within a spatial framework can provide a strong approach to understanding community structure and dynamics, while explaining patterns of species diversity.