skip to main content


Title: Ecology eclipses phylogeny as a major driver of nematode parasite community structure in a graminivorous primate
Abstract

Understanding how ecology and phylogeny shape parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.

We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.

We characterized the gastrointestinal (GI) parasite community of wild geladasTheropithecus gelada, primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands.

Geladas exhibited very constrained GI parasite communities: only two genera (OesophagostomumandTrichostrongylus) were identified across 305 samples. This is far below the diversity reported for baboons (Papiospp.) and at the low end of the range of domestic grazers (e.g.Bos taurus,Ovis aries) inhabiting the same region and ecological niche.

Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched toOesophagostomumsp., seven toTrichostrongylussp., and one toT. vitrinus.

Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited approximately four times higher ASV richness than geladas at a less disturbed location within the park.

In this system, ecology was a stronger predictor of parasite community structure than was phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa.

A freePlain Language Summarycan be found within the Supporting Information of this article.

 
more » « less
Award ID(s):
1854359 1255974 0715179 2013888
NSF-PAR ID:
10456867
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Functional Ecology
Volume:
34
Issue:
9
ISSN:
0269-8463
Page Range / eLocation ID:
p. 1898-1906
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Hosts and their parasites exist within complex ecological communities. However, the role that non‐focal community members, species which cannot be infected by a focal pathogen, may play in altering parasite transmission is often only studied in the lens of the ‘diversity‐disease’ relationship by focusing on species richness. This approach largely ignores mechanistic species interactions and risks collapsing our understanding of the community ecology of disease down to defining the prominence of ‘amplification’ versus ‘dilution’ effects.

    However, non‐focal species vary in their traits, densities and types of interactions with focal hosts and parasites. Therefore, a community ecology approach based on the mechanisms underlying parasite transmission, host harm and dynamic species interactions may better advance our understanding of parasite transmission in complex communities.

    Using the concept of the parasite's basic reproductive ratio,R0, as a generalizable framework, we examine several critical mechanisms by which interactions among hosts, parasites and non‐focal species modulate transmission and provide examples from relevant literature.

    By focusing on the mechanism by which non‐focal species impact transmission, we can emphasize the similarities among classic paradigms in the community ecology of disease, gain new insights into parasite invasion and persistence, better predict community traits correlated with disease dilution or amplification, and gauge the feasibility of biocontrol for parasites of conservation, agricultural or human health concern.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  2. Abstract

    Megafauna assemblages have declined or disappeared throughout much of the world, and many efforts are underway to restore them. Understanding the trophic ecology of such reassembling systems is necessary for predicting recovery dynamics, guiding management, and testing general theory. Yet, there are few studies of recovering large‐mammal communities, and fewer still that have characterized food‐web structure with high taxonomic resolution.

    In Gorongosa National Park, large herbivores have rebounded from near‐extirpation following the Mozambican Civil War (1977–1992). However, contemporary community structure differs radically from the prewar baseline: medium‐sized ungulates now outnumber larger bodied species, and several apex carnivores remain locally extinct.

    We used DNA metabarcoding to quantify diet composition of Gorongosa’s 14 most abundant large‐mammal populations. We tested five hypotheses: (i) the most abundant populations exhibit greatest individual‐level dietary variability; (ii) these populations also have the greatest total niche width (dietary diversity); (iii) interspecific niche overlap is high, with the diets of less‐abundant species nested within those of more‐abundant species; (iv) partitioning of forage species is stronger in more structurally heterogeneous habitats; and (v) selectivity for plant taxa converges within guilds and digestive types, but diverges across them.

    Abundant (and narrow‐mouthed) populations exhibited higher among‐individual dietary variation, but not necessarily the greatest dietary diversity. Interspecific dietary overlap was high, especially among grazers and in structurally homogenous habitat, whereas niche separation was more pronounced among browsers and in heterogeneous habitat. Patterns of selectivity were similar for ruminants—grazers and browsers alike—but differed between ruminants and non‐ruminants.

    Synthesis. The structure of this recovering food web was consistent with several hypotheses predicated on competition, habitat complexity, and herbivore traits, but it differed from patterns observed in more intact assemblages. We propose that intraspecific competition in the fastest‐recovering populations has promoted individual variation and a more nested food web, wherein rare species use subsets of foods eaten by abundant species, and that this scenario is reinforced by weak predation pressure. Future work should test these conjectures and analyse how the taxonomic dietary niche axis studied here interacts with other mechanisms of diet partitioning to affect community reassembly following wildlife declines.

     
    more » « less
  3. Abstract

    Helminth parasites can have wide‐ranging, detrimental effects on host reproduction and survival. These effects are best documented in humans and domestic animals, while only a few studies in wild mammals have identified both the forces that drive helminth infection risk and their costs to individual fitness.

    Working in a well‐studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya, we pursued two goals, to (a) examine the costs of helminth infections in terms of female fertility and glucocorticoid hormone levels and (b) test how processes operating at multiple scales—from individual hosts to social groups and the population at large—work together to predict variation in female infection risk.

    To accomplish these goals, we measured helminth parasite burdens in 745 faecal samples collected over 5 years from 122 female baboons. We combine these data with detailed observations of host environments, social behaviours, hormone levels and interbirth intervals (IBIs).

    We found that helminths are costly to female fertility: females infected with more diverse parasite communities (i.e., higher parasite richness) exhibited longer IBIs than females infected by fewer parasite taxa. We also found that females exhibiting highTrichuris trichiuraegg counts also had high glucocorticoid levels. Female infection risk was best predicted by factors at the host, social group and population level: females facing the highest risk were old, socially isolated, living in dry conditions and infected with other helminths.

    Our results provide an unusually holistic understanding of the factors that contribute to inter‐individual differences in parasite infection, and they contribute to just a handful of studies linking helminths to host fitness in wild mammals.

     
    more » « less
  4. Abstract

    In an era of anthropogenically altered disturbance regimes and increased nutrient loads, understanding how communities respond to these perturbations is essential for successful habitat restoration. Disturbance and resource supply can affect community diversity by altering community assembly processes, such as recruitment, mortality or competitive inequalities. The mechanisms behind community responses to these drivers will differentially affect multiple facets of diversity.

    Here we examine how factorial manipulations of disturbance (raking to remove above‐ground vegetation) and nitrogen supply affect taxonomic and phylogenetic diversity of predominantly annual California grassland communities spanning a 500‐km latitudinal and twofold rainfall gradient. The disturbance caused density‐independent biomass removal and increased access to resources such as space and light, thus mimicking demographic effects of disturbance as considered in ecological models and broadly applicable to empirical systems. We used paired metrics of richness, evenness and community composition to compare evidence from taxonomy and phylogeny.

    Disturbance increased species and phylogenetic diversity (richness and evenness metrics). However, nitrogen addition interacted with disturbance to reduce species richness and phylogenetic diversity. Undisturbed communities were more strongly clustered phylogenetically, but disturbance eroded this clustering such that communities became more random (i.e. indistinguishable from a null model of assembly). Species composition differed between disturbed and undisturbed communities, and many species were observed in only one community type. Disturbance interacted with nitrogen supply to alter phylogenetic composition of communities, and recently disturbed communities were more spatially variable in phylogenetic composition than undisturbed communities. Phylogenetic composition of communities also differed among nitrogen treatments.

    Synthesis.Our results suggest that disturbing these grassland communities by removing above‐ground vegetation increased community diversity by increasing recruitment. Seed addition following this type of disturbance is thus likely to be an effective restoration technique. However, we have shown that disturbance combined with nitrogen enrichment reduces community diversity. The mechanism for this enrichment effect does not appear to be linked to increased productivity leading to light limitation. This work suggests restoration efforts employing biomass removal must take nutrient availability into account to maximize local community diversity.

     
    more » « less
  5. Abstract

    Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector‐transmitted parasites.

    Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity ofLeucocytozoon(an avian blood parasite) at site and species levels across the New World.

    To explore spatial patterns in infection probability and lineage diversity forLeucocytozoonparasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high‐resolution satellite remote‐sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly.

    Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence ofLeucocytozoonparasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected withLeucocytozoonincreased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes.

    Whereas temperature partially constrainsLeucocytozoondiversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, forLeucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector‐transmitted parasites. Unlike other vector‐transmitted diseases, our results show thatLeucocytozoondiversity and prevalence will likely decrease with warming temperatures.

     
    more » « less