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Their young bite better: On- and off-host selection pressure as drivers for evolutionary-developmental modification in Rhipicephalus ticks

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Abstract

Distinct life stages may experience different selection pressures influencing phenotypic evolution. Morphological evolution is also constrained by early phenotypes, since early development forms the phenotypic basis of later development. This work investigates evolutionary-developmental modification in three life stages and both sexes of 24 Rhipicephalus species using phylogenetic comparative methods for geometric morphometrics of basis capituli (basal mouthpart structure used for host attachment), and scutum or conscutum areas (proxy for overall body size). Findings indicate species using large hosts at early life stages have distinct basis capituli shapes, correlated with host size, enabling attachment to the tough skins of large hosts. Host-truncate species (one- and two-host) generally retain these adaptive features into later life stages, suggesting neoteny is linked to the evolution of host truncation. In contrast, species using small hosts at early life stages have lost these features. Developmental trajectories differ significantly between host-use strategies (niches), and correlate with distinct clades. In two-host and three-host species using large hosts at early life stages, developmental change is heterotopically accelerated (greater cell mass development) before the first off-host period where selection probably favours large individuals able to better resist dehydration when questing (waiting) for less abundant, less active hosts. In other species, development is heterotopically reduced (neotenic), possibly because dehydration risk is bypassed by prolonged host attachment (one-host species – heterotopic neoteny), or is allometrically repatterned possibly by using highly abundant and active hosts (three-host species using small hosts at early life stages – allometric repatterning). These findings highlight complex trade-offs between on- and off-host factors of free-living ectoparasite ecology, which mediate responses to diverse selection pressures varied by life stage and host-use strategy. It is proposed that these trade-offs shape evolutionary-developmental morphology and diversity of Rhipicephalus ticks.

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Ticks in the genus Rhipicephalus include many important vectors of animal and human pathogens, but many species are notoriously difficult to identify, particularly as immature stages. This reference volume provides identification keys for adult ticks from the Afrotropical regions and elsewhere. For the nymphs and larvae, unique plates have been compiled in which line drawings of the capitula of similar species are grouped together to facilitate identification. Brief well-illustrated descriptions of the known stages of every species are given, plus information on their hosts, distribution, and disease relationships. Tables providing data on host/parasite relationships and disease transmission are also included, making this the definitive reference source on this group for all those interested in acarology, veterinary or medical parasitology and entomology for many years to come.
Article
Quantitative analyses of morphological variation using geometric morphometrics are often performed on 2D photos of 3D structures. It is generally assumed that the error due to the flattening of the third dimension is negligible. However, despite hundreds of 2D studies, few have actually tested this assumption and none has done it on large animals, such as those typically classified as megafauna. We explore this issue in living equids, focusing on ventral cranial variation at both micro- and macro-evolutionary levels. By comparing 2D and 3D data, we found that size is well approximated, whereas shape is more strongly impacted by 2D inaccuracies, as it is especially evident in intra-specific analyses. The 2D approximation improves when shape differences are larger, as in macroevolution, but even at this level precise inter-individual similarity relationships are altered. Despite this, main patterns of sex, species and allometric variation in 2D were the same as in 3D, thus suggesting that 2D may be a source of 'noise' that does not mask the main signal in the data. However, the picture that emerges from this and other recent studies on 2D approximation of 3D structures is complex and any generalization premature. Morphometricians should therefore test the appropriateness of 2D using preliminary investigations in relation to the specific study questions in their own samples. We discuss whether this might be feasible using a reduced landmark configuration and smaller samples, which would save time and money. In an exploratory analysis, we found that in equids results seem robust to sampling, but become less precise and, with fewer landmarks, may slightly overestimate 2D inaccuracies.
Article
XYOM, for XY Online Morphometrics, is an online implementation of the geometric morphometric (GM) approach. It is a platform-independent product, and is presented here as an optional alternative software to client side morphometrics software. From the point of view of the user, the interesting features of a web application are: no download, no installation, no configuration, and automatic updating. Because XYOM is accessible through a standard web interface, it is expected to allow an easier and faster learning process. Additional benefits are that users will have their own highly secured cloud storage, with a 24/7 access from any device, allowing users to share their data, export/download them into their device. Ideally, there would be a permanent, anywhere anytime access on any device (computer, tablet, smartphone, etc). Using modern web browsers, XYOM allows online 2D images digitization of either landmarks, semilandmarks or pseudolandmarks (contours), and develops corresponding statistical analyses. In its present configuration, XYOM is dedicated to the identification and characterization of organismal forms.
Article
The systematics of the genera and subgenera within the soft tick family Argasidae is not adequately resolved. Different classification schemes, reflecting diverse schools of scientific thought that elevated or downgraded groups to genera or subgenera, have been proposed. In the most recent classification scheme, Argas and Ornithodoros are paraphyletic and the placement of various subgenera remains uncertain because molecular data are lacking. Thus, reclassification of the Argasidae is required. This will enable an understanding of soft tick systematics within an evolutionary context. This study addressed that knowledge gap using mitochondrial genome and nuclear (18S and 28S ribosomal RNA) sequence data for representatives of the subgenera Alectorobius, Argas, Chiropterargas, Ogadenus, Ornamentum, Ornithodoros, Navis (subgen. nov.), Pavlovskyella, Persicargas, Proknekalia, Reticulinasus and Secretargas, from the Afrotropical, Nearctic and Palearctic regions. Hard tick species (Ixodidae) and a new representative of Nuttalliella namaqua (Nuttalliellidae), were also sequenced with a total of 83 whole mitochondrial genomes, 18S rRNA and 28S rRNA genes generated. The study confirmed the utility of next-generation sequencing to retrieve systematic markers. Paraphyly of Argas and Ornithodoros was resolved by systematic analysis and a new species list is proposed. This corresponds broadly with the morphological cladistic analysis of Klompen and Oliver (1993). Estimation of divergence times using molecular dating allowed dissection of phylogeographic patterns for argasid evolution. The discovery of cryptic species in the subgenera Chiropterargas, Ogadenus and Ornithodoros, suggests that cryptic speciation is common within the Argasidae. Cryptic speciation has implications for past biological studies of soft ticks. These are discussed in particular for the Ornithodoros (Ornithodoros) moubata and Ornithodoros (Ornithodoros) savignyi groups.
Book
This is a comprehensive work summarizing the current state of knowledge of the biology of the hard ticks (Acari: Ixodidae) of Southern Africa (South Africa, Namibia, Botswana, Swaziland, Lesotho and Maputo Province, Mozambique). It provides an overview of the history of tick research in Southern Africa and the evolution of our knowledge of the ticks’ distribution and biology, as well as the methods used to determine tick distribution, abundance and host preference. The morphologies of most of the tick species known to occur in Southern Africa are described and illustrated, and their distributions are described and mapped in relation to the biomes of the region. The known hosts for each tick species are listed, and the tick’s host preferences are discussed. Information on most species life cycle in the laboratory and the field, and their seasonal occurrence, is summarized. The diseases of animals and humans transmitted or caused by each tick species are summarized in relation to tick ecology. Aspects of the biology of the major hosts relevant to tick infestations are described, and extensive tick/host and host/tick lists are provided for each country
Article
An adaptationist programme has dominated evolutionary thought in England and the United States during the past 40 years. It is based on faith in the power of natural selection as an optimizing agent. It proceeds by breaking an oragnism into unitary 'traits' and proposing an adaptive story for each considered separately. Trade-offs among competing selective demands exert the only brake upon perfection; non-optimality is thereby rendered as a result of adaptation as well. We criticize this approach and attempt to reassert a competing notion (long popular in continental Europe) that organisms must be analysed as integrated wholes, with Baupläne so constrained by phyletic heritage, pathways of development and general architecture that the constraints themselves become more interesting and more important in delimiting pathways of change than the selective force that may mediate change when it occurs. We fault the adaptationist programme for its failure to distinguish current utility from reasons for origin (male tyrannosaurs may have used their diminutive front legs to titillate female partners, but this will not explain why they got so small); for its unwillingness to consider alternatives to adaptive stories; for its reliance upon plausibility alone as a criterion for accepting speculative tales; and for its failure to consider adequately such competing themes as random fixation of alleles, production of non-adaptive structures by developmental correlation with selected features (allometry, pleiotropy, material compensation, mechanically forced correlation), the separability of adaptation and selection, multiple adaptive peaks, and current utility as an epiphenomenon of non-adaptive structures. We support Darwin's own pluralistic approach to identifying the agents of evolutionary change.
Article
Heterochrony, change in developmental rate and timing, is widely recognized as an agent of evolutionary change. Heterotopy, evolutionary change in spatial patterning of development, is less widely known or understood. Although Haeckel coined the term as a complement to heterochrony in 1866, few studies have detected heterotopy or even considered the possibility that it might play a role in morphological evolution. We here review the roles of heterochrony and heterotopy in evolution and discuss how they can be detected. Heterochrony is of interest in part because it can produce novelties constrained along ancestral ontogenies, and hence result in parallelism between ontogeny and phylogeny. Heterotopy can produce new morphologies along trajectories different from those that generated the forms of ancestors. We argue that the study of heterochrony has been bound to an analytical formalism that virtually precludes the recognition of heterotopy, so we provide a new framework for the construction of ontogenetic trajectories and illustrate their analysis in a phylogenetic context. The study of development of form needs tools that capture not only rates of development but the space in which the changes are manifest. The framework outlined here provides tools applicable to both. When appropriate tools are used and the necessary steps are taken, a more comprehensive interpretation of evolutionary change in development becomes possible. We suspect that there will be very few cases of change solely in developmental rate and timing or change solely in spatial patterning; most ontogenies evolve by changes of spatiotemporal pattern.
Article
Resistance to Rhipicephalus microplus infestation in cattle has many effector mechanisms, each of which is likely to be modulated by complex, interacting factors. Some of the mechanisms of host resistance and their modulating factors have been identified and quantified, although much remains to be explained. The variation in resistance to tick infestation is most marked between Bos taurus and Bos indicus cattle, taurine cattle given the same exposure carrying between five and ten times as many ticks as indicine cattle. Tick resistance is mostly manifest against attaching larvae, which attempt to feed often and without success, death occurring mostly within 24 h of finding a host. There is evidence of innate and adaptive immune response to tick infestation and it appears that the relative importance of each differs between indicine and taurine cattle. There is conflicting information regarding the role of humoral immunity in tick resistance, recent studies indicating that strong IgG responses to tick antigens are not protective. A strong T-cell mediated response directed against larval stages, as mounted by indicine cattle, seems to be protective. Variation in the extracellular matrix of skin (epidermal growth factors, collagens and other matrix components such as lumican) also contributes to variation in host resistance.This article is protected by copyright. All rights reserved.
Article
This paper considers the effect of stochasticity on the quality of convergence of genetic algorithms (GAs). In many problems, the variance of building-block fitness or so-called collateral noise is the major source of variance, and a population-sizing equation is derived to ensure that average signal-to-collateral-noise ratios are favorable to the discrimination of the best building blocks required to solve a problem of bounded deception. The sizing relation is modified to permit the inclusion of other sources of stochasticity, such as the noise of selection, the noise of genetic operators, and the explicit noise or nondeterminism of the objective function. In a test suite of five functions, the sizing relation proves to be a conservative predictor of average correct convergence, as long as all major sources of noise are considered in the sizing calculation. These results suggest how the sizing equation may be viewed as a coarse delineation of a boundary between what a physicist might call two distinct phases of GA behavior. At low population sizes the GA makes many errors of decision, and the quality of convergence is largely left to the vagaries of chance or the serial fixup of flawed results through mutation or other serial injection of diversity. At large population sizes, GAs can reliably discriminate between good and bad building blocks, and parallel processing and recombination of building blocks lead to quick solution of even difficult deceptive problems. Additionally, the paper outlines a number of extensions to this work, including the development of more refined models of the relation between generational average error and ultimate convergence quality, the development of online methods for sizing populations via the estimation of population-s...
Article
1. Here, I present a new, multifunctional phylogenetics package, phytools, for the R statistical computing environment. 2. The focus of the package is on methods for phylogenetic comparative biology; however, it also includes tools for tree inference, phylogeny input/output, plotting, manipulation and several other tasks. 3. I describe and tabulate the major methods implemented in phytools, and in addition provide some demonstration of its use in the form of two illustrative examples. 4. Finally, I conclude by briefly describing an active web-log that I use to document present and future developments for phytools. I also note other web resources for phylogenetics in the R computational environment.
Article
Increasingly, data on shape are analysed in combination with molecular genetic or ecological information, so that tools for geometric morphometric analysis are required. Morphometric studies most often use the arrangements of morphological landmarks as the data source and extract shape information from them by Procrustes superimposition. The MorphoJ software combines this approach with a wide range of methods for shape analysis in different biological contexts. The program offers an integrated and user-friendly environment for standard multivariate analyses such as principal components, discriminant analysis and multivariate regression as well as specialized applications including phylogenetics, quantitative genetics and analyses of modularity in shape data. MorphoJ is written in Java and versions for the Windows, Macintosh and Unix/Linux platforms are freely available from http://www.flywings.org.uk/MorphoJ_page.htm.
Book
This book has been designed to summarize current, essential information for every one of the world's 700+ hard tick species. Under each species name, we will cite the original description, followed by information on type depositories, known stages, distribution (by zoogeographic region and ecoregion), hosts, and human infestation (if any). Each species account will also include a list of salient references and, where necessary, remarks on systematic status. We envision eight chapters: six devoted to the major ixodid tick genera (Amblyomma, Dermacentor, Haemaphysalis, Hyalomma, Ixodes, Rhipicephalus), one covering eight minor genera (including two that are fossil), and a concluding summary chapter. There will be two tables on host associations and zoogeography in each major genus chapter, as well as five tables in the summary chapter, for a total of 17 tables. No similar synopsis of the world's hard tick species exists in any language. © 2014 Springer Science+Business Media Dordrecht. All rights are reserved.
Article
The tick Ixodes ricinus uses its mouthparts to penetrate the skin of its host and to remain attached for about a week, during which time Lyme disease spirochaetes may pass from the tick to the host. To understand how the tick achieves both tasks, penetration and attachment, with the same set of implements, we recorded the insertion events by cinematography, interpreted the mouthparts' function by scanning electron microscopy and identified their points of articulation by confocal microscopy. Our structural dynamic observations suggest that the process of insertion and attachment occurs via a ratchet-like mechanism with two distinct stages. Initially, the two telescoping chelicerae pierce the skin and, by moving alternately, generate a toehold. Subsequently, a breaststroke-like motion, effected by simultaneous flexure and retraction of both chelicerae, pulls in the barbed hypostome. This combination of a flexible, dynamic mechanical ratchet and a static holdfast thus allows the tick to solve the problem of how to penetrate skin and also remain stuck for long periods of time.
Article
Effect size helps readers understand the magnitude of differences found, whereas statistical significance examines whether the findings are likely to be due to chance. Both are essential for readers to understand the full impact of your work. Report both in the Abstract and Results sections.