Sensitivity of bipartite network analyses to incomplete sampling and taxonomic uncertainty.

Bipartite network analysis is a powerful tool to study the processes structuring interactions in ecological communities. In applying the method, it is assumed that the sampled interactions provide an accurate representation of the actual community. However, acquiring a representative sample may be difficult as not all species are equally abundant or easily identifiable. Two potential sampling issues can compromise the conclusions of bipartite network analyses: failure to capture the full range of interactions (sampling completeness) and use of a taxonomic level higher than species to evaluate the network (taxonomic resolution). We asked how commonly used descriptors of bipartite antagonistic communities (modularity, nestedness, connectance, and specialization [H2 ']) are affected by reduced host sampling completeness, parasite taxonomic resolution, and their crossed effect, as they are likely to co-occur. We used a quantitative niche model to generate weighted bipartite networks that resembled natural host-parasite communities. The descriptors were more sensitive to uncertainty in parasite taxonomic resolution than to host sampling completeness. When only 10% of parasite taxonomic resolution was retained, modularity and specialization decreased by ~76% and ~12%, respectively, and nestedness and connectance increased by ~114% and ~345% respectively. The loss of taxonomic resolution led to a wide range of possible communities, which made it difficult to predict its effects on a given network. With regards to host sampling completeness, standardized nestedness, connectance, and specialization were robust, whereas modularity was sensitive (~30% decrease). The combination of both sampling issues had an additive effect on modularity. In communities with low effort for both sampling issues (50%-10% of sampling completeness and taxonomic resolution), estimators of modularity, and nestedness could not be distinguished from those of random assemblages. Thus, the categorical description of communities with low sampling effort (e.g., if a community is modular or not) should be done with caution. We recommend evaluating both sampling completeness and taxonomic certainty when conducting bipartite network analyses. Care should also be exercised when using nonrobust descriptors (the four descriptors for parasite taxonomic resolution; modularity for host sampling completeness) when sampling issues are likely to affect a dataset.

Network Analysis: Ten Years Shining Light on Host-Parasite Interactions.

Biological interactions are key drivers of ecological and evolutionary processes. The complexity of such interactions hinders our understanding of ecological systems and our ability to make effective predictions in changing environments. However, network analysis allows us to better tackle the complexity of ecosystems because it extracts the properties of an ecological system according to the number and distribution of links among interacting entities. The number of studies using network analysis to solve ecological and evolutionary questions in parasitology has increased over the past decade. Here, we synthesise the contribution of network analysis toward disentangling host-parasite processes. Furthermore, we identify current trends in mainstream ecology and novel applications of network analysis that present opportunities for research on host-parasite interactions.

Assembly rules of helminth parasite communities in grey mullets: combining components of diversity.

Organisms aggregate in ecological communities. It has been widely debated whether these associations are explained by deterministic or, in contrast, random processes. The answer may vary, depending on the level of an organisational scale (α, ß and γ) and the facet of diversity considered: taxonomic, functional and phylogenetic. Diversity at the level of a sampling unit (i.e. host individual) is the α diversity; ß diversity represents the extent of dissimilarity in diversity among sampling units (within a level of an organisational scale, ß1; between levels of an organisational scale, ß2); and the total diversity of a system is γ diversity. Thus, the combination of facets and levels of a scale may be useful to disentangle the mechanisms driving the composition of a parasite community. Using helminth parasite taxonomic, functional, and a proxy for phylogenetic diversity of three species of grey mullets (Teleostei: Mugilidae) from the Mediterranean Sea, we show that random and deterministic processes of different nature explain the assemblage of parasite communities. The parasite community at a host individual (α) was invariably a random subset of the total diversity in the community for the three facets of diversity. At the ß1 level, taxonomic diversity was lower than expected by chance, whereas functional diversity and the proxy for phylogenetic diversity were random. At the ß2 level, diversity patterns suggested environmental filtering of the parasite assemblage: species, trait, and phylogenetic compositions of parasite communities seemed to depend primarily on the species of host, but also on the locality and season. Our study shows that parasite communities are not totally understood if any of the components (i.e. facets and levels) of diversity is neglected.

Random Tanglegram Partitions (Random TaPas): An Alexandrian Approach to the Cophylogenetic Gordian Knot.

Symbiosis is a key driver of evolutionary novelty and ecological diversity, but our understanding of how macroevolutionary processes originate extant symbiotic associations is still very incomplete. Cophylogenetic tools are used to assess the congruence between the phylogenies of two groups of organisms related by extant associations. If phylogenetic congruence is higher than expected by chance, we conclude that there is cophylogenetic signal in the system under study. However, how to quantify cophylogenetic signal is still an open issue. We present a novel approach, Random Tanglegram Partitions (Random TaPas) that applies a given global-fit method to random partial tanglegrams of a fixed size to identify the associations, terminals, and nodes that maximize phylogenetic congruence. By means of simulations, we show that the output value produced is inversely proportional to the number and proportion of cospeciation events employed to build simulated tanglegrams. In addition, with time-calibrated trees, Random TaPas can also distinguish cospeciation from pseudocospeciation. Random TaPas can handle large tanglegrams in affordable computational time and incorporates phylogenetic uncertainty in the analyses. We demonstrate its application with two real examples: passerine birds and their feather mites, and orchids and bee pollinators. In both systems, Random TaPas revealed low cophylogenetic signal, but mapping its variation onto the tanglegram pointed to two different coevolutionary processes. We suggest that the recursive partitioning of the tanglegram buffers the effect of phylogenetic nonindependence occurring in current global-fit methods and therefore Random TaPas is more reliable than regular global-fit methods to identify host-symbiont associations that contribute most to cophylogenetic signal. Random TaPas can be implemented in the public-domain statistical software R with scripts provided herein. A User's Guide is also available at GitHub.[Codiversification; coevolution; cophylogenetic signal; Symbiosis.].

Towards a Unified Functional Trait Framework for Parasites.

Trait-based research holds high potential to unveil ecological and evolutionary processes. Functional traits are fitness-related characteristics of individuals, which are measured at individual level and defined without using information external to the individual. Despite the usefulness of the functional approach to understand the performance of individuals in ecosystems, and parasitism being the most common life-history strategy on Earth, studies based on functional traits of parasites are still scarce. Since the choice of functional traits is a critical step for any study, we propose a core list of seven functional traits of metazoan parasites, related to three universal challenges faced by organisms (dispersal, establishment, and persistence), and give guidelines to define appropriate functional traits in future parasite community studies.

Author Correction: Evaluation of three methods for biomass estimation in small invertebrates, using three large disparate parasite species as model organisms.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Evaluation of three methods for biomass estimation in small invertebrates, using three large disparate parasite species as model organisms.

Invertebrate biomass is considered one of the main factors driving processes in ecosystems. It can be measured directly, primarily by weighing individuals, but more often indirect estimators are used. We developed two indirect and non-destructive approaches to estimate biomass of small invertebrates in a simple manner. The first one was based on clay modelling and the second one was based on image analysis implemented with open-source software. Furthermore, we tested the accuracy of the widely used geometric approximation method (third method). We applied these three different methods to three morphologically disparate model species, an acanthocephalan worm, a crustacean and a flatworm. To validate our indirect estimations and to test their accuracy, we weighed specimens of the three species and calculated their tissue densities. Additionally, we propose an uncomplicated technique to estimate thickness of individuals under a microscope, a required measurement for two of the three indirect methods tested. The indirect methods proposed in this paper provided the best approximation to direct measurements. Despite its wide use, the geometric approximation method showed the lowest accuracy. The approaches developed herein are timely because the recently increasing number of studies requiring reliable biomass estimates for small invertebrates to explain crucial processes in ecosystems.

Phenotypic Buffering in a Monogenean: Canalization and Developmental Stability in Shape and Size of the Haptoral Anchors of Ligophorus cephali (Monogenea: Dactylogyridae).

Phenotypic variation results from the balance between sources of variation and counteracting regulatory mechanisms. Canalization and developmental stability are two such mechanisms, acting at two different levels of regulation. The issue of whether or not they act concurrently as a common developmental buffering capacity has been subject to debate. We used geometric morphometrics to quantify the mechanisms that guarantee phenotypic constancy in the haptoral anchors of Ligophorus cephali. Canalization and developmental stability were appraised by estimating inter- and intra-individual variation, respectively, in size and shape of dorsal and ventral anchors. The latter variation was estimated as fluctuating asymmetry (FA) between anchor pairs. The general-buffering-capacity hypothesis was tested by two different methods based on correlations and Principal Components Analyses of the different components of size and shape variation. Evidence for FA in the dorsal and ventral anchors in both shape and size was found. Our analyses supported the hypothesis of a general developmental buffering capacity. The evidence was more compelling for shape than for size and, particularly, for the ventral anchors than for the dorsal ones. These results are in line with previous studies of dactylogyrids suggesting that ventral anchors secure a firmer, more permanent attachment, whereas dorsal anchors are more mobile. Because fixation to the host is crucial for survival in ectoparasites, we suggest that homeostatic development of the ventral anchors has been promoted to ensure the morphological constancy required for efficient attachment. Geometric morphometrics can be readily applied to other host-monogenean models, affording not only to disentangle the effects of canalization and developmental stability, as shown herein, but to further partition the environmental and genetic components of the former.

A New Species of Ligophorus (Monogenea: Dactylogyridae) from the gills of the Flathead Mullet Mugil cephalus (Teleostei: Mugilidae) from Mexico.

A new monogenean species, Ligophorus yucatanensis n. sp. from the gills of the flathead mullet Mugil cephalus from the Yucatan Peninsula, Mexico, is described. The new species can be differentiated from all other species of Ligophorus by the morphology of the accessory piece of the copulatory organ. Its main lobe is cylindrical, tunnelled expanded distally, slightly bowed with a characteristic membranous opening at level of medial bifurcation of the accessory piece, forming a thick-walled bulbshaped expansion that ends in a round labium. The secondary lobe is spatulate, straight, and shorter than the main lobe. In addition, the new species can be distinguished from other species by the morphology of the haptoral ventral bar, and the distal end of the vaginal duct. Furthermore the ventral anchors are shorter than those of all other species of Ligophorus reported in the Gulf of Mexico and Caribbean Sea. In addition, the zoogeographical records of Ligophorus spp. on the M. cephalus species complex are briefly reviewed and updated.

Phenotypic plasticity in haptoral structures of Ligophorus cephali (Monogenea: Dactylogyridae) on the flathead mullet (Mugil cephalus): a geometric morphometric approach.

Evaluating phenotypic plasticity in attachment organs of parasites can provide information on the capacity to colonise new hosts and illuminate evolutionary processes driving host specificity. We analysed the variability in shape and size of the dorsal and ventral anchors of Ligophorus cephali from Mugil cephalus by means of geometric morphometrics and multivariate statistics. We also assessed the morphological integration between anchors and between the roots and points in order to gain insight into their functional morphology. Dorsal and ventral anchors showed a similar gradient of overall shape variation, but the amount of localised changes was much higher in the former. Statistical models describing variations in shape and size revealed clear differences between anchors. The dorsal anchor/bar complex seems more mobile than the ventral one in Ligophorus, and these differences may reflect different functional roles in attachment to the gills. The lower residual variation associated with the ventral anchor models suggests a tighter control of their shape and size, perhaps because these anchors seem to be responsible for firmer attachment and their size and shape would allow more effective responses to characteristics of the microenvironment within the individual host. Despite these putative functional differences, the high level of morphological integration indicates a concerted action between anchors. In addition, we found a slight, although significant, morphological integration between roots and points in both anchors, which suggests that a large fraction of the observed phenotypic variation does not compromise the functional role of anchors as levers. Given the low level of genetic variation in our sample, it is likely that much of the morphological variation reflects host-driven plastic responses. This supports the hypothesis of monogenean specificity through host-switching and rapid speciation. The present study demonstrates the potential of geometric morphometrics to provide new and previously unexplored insights into the functional morphology of attachment and evolutionary processes of host-parasite coevolution.