Evolution of complex life cycles in trophically transmitted helminths. I. Host incorporation and trophic ascent

Links between parasites and food webs are evolutionarily ancient but dynamic: life history theory provides insights into helminth complex life cycle origins. Most adult helminths benefit by sexual reproduction in vertebrates, often high up food chains, but direct infection is commonly constrained by a trophic vacuum between free‐living propagules and definitive hosts. Intermediate hosts fill this vacuum, facilitating transmission to definitive hosts. The central question concerns why sexual reproduction, and sometimes even larval growth, is suppressed in intermediate hosts, favouring growth arrest at larval maturity in intermediate hosts and reproductive suppression until transmission to definitive hosts? Increased longevity and higher growth in definitive hosts can generate selection for larger parasite body size and higher fecundity at sexual maturity. Life cycle length is increased by two evolutionary mechanisms, upward and downward incorporation, allowing simple (one‐host) cycles to become complex (multihost). In downward incorporation, an intermediate host is added below the definitive host: models suggest that downward incorporation probably evolves only after ecological or evolutionary perturbations create a trophic vacuum. In upward incorporation, a new definitive host is added above the original definitive host, which subsequently becomes an intermediate host, again maintained by the trophic vacuum: theory suggests that this is plausible even under constant ecological/evolutionary conditions. The final cycle is similar irrespective of its origin (upward or downward). Insights about host incorporation are best gained by linking comparative phylogenetic analyses (describing evolutionary history) with evolutionary models (examining selective forces). Ascent of host trophic levels and evolution of optimal host taxa ranges are discussed.     

The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths

Parasitic worms (helminths) frequently have complex life cycles in which they are transmitted trophically between two or more successive hosts. Sexual reproduction often takes place in high trophic-level (TL) vertebrates, where parasites can grow to large sizes with high fecundity. Direct infection of high TL hosts, while advantageous, may be unachievable for parasites constrained to transmit trophically, because helminth propagules are unlikely to be ingested by large predators. Lack of niche overlap between propagule and definitive host (the trophic transmission vacuum) may explain the origin and/or maintenance of intermediate hosts, which overcome this transmission barrier. We show that nematodes infecting high TL definitive hosts tend to have more successive hosts in their life cycles. This relationship was modest, though, driven mainly by the minimum TL of hosts, suggesting that the shortest trophic chains leading to a host define the boundaries of the transmission vacuum. We also show that alternative modes of transmission, like host penetration, allow nematodes to reach high TLs without intermediate hosts. We suggest that widespread omnivory as well as parasite adaptations to increase transmission probably reduce, but do not eliminate, the barriers to the transmission of helminths through the food web.     

Evolution of extreme body size disparity in monitor lizards (Varanus)

Many features of species' biology, including life history, physiology, morphology, and ecology are tightly linked to body size. Investigation into the causes of size divergence is therefore critical to understanding the factors shaping phenotypic diversity within clades. In this study, we examined size evolution in monitor lizards (Varanus), a clade that includes the largest extant lizard species, the Komodo dragon (V. komodoensis), as well as diminutive species that are nearly four orders of magnitude smaller in adult body mass. We demonstrate that the remarkable body size disparity of this clade is a consequence of different selective demands imposed by three major habitat use patterns-arboreality, terrestriality, and rock-dwelling. We reconstructed phylogenetic relationships and ancestral habitat use and applied model selection to determine that the best-fitting evolutionary models for species' adult size are those that infer oppositely directed adaptive evolution associated with terrestriality and rock-dwelling, with terrestrial lineages evolving extremely large size and rock-dwellers becoming very small. We also show that habitat use affects the evolution of several ecologically important morphological traits independently of body size divergence. These results suggest that habitat use exerts a strong, multidimensional influence on the evolution of morphological size and shape disparity in monitor lizards.     

The role of ecological constraint in driving the evolution of avian song frequency across a latitudinal gradient

Just as features of the physical and biotic environment constrain evolution of ecological and morphological traits, they may also affect evolution of communication systems. Here we analyze constraints on rates of vocal evolution, using a large dataset of New World avian sister taxa. We show that species breeding in tropical forests sing at generally lower frequencies and across narrower bandwidths than species breeding in open habitats, or at high latitudes. We attribute these restrictions on birdsong frequency to the presence of high-frequency insect noise and greater degradation of high-frequency sounds in tropical forests. We fit Ornstein-Uhlenbeck models to show that recent evolution of song frequency has been more greatly constrained in tropical forests than elsewhere, that is, songs have shown less tendency to diverge over time in tropical forests, consistent with inferred acoustic restrictions. In addition, we find that song frequency has evolved more rapidly overall at high latitudes in both forest and open habitats. Besides a larger available sound window, other factors contributing to more rapid divergence at high latitudes may include an overall increased intensity of sexual selection, occupation of more divergent habitats, and the presence of fewer competing species.     

Variation in the trophic basis of production and energy flow associated with emergence of larval salamander assemblages from forest ponds

1. Larval amphibians are a dominant consumer in many freshwater systems, yet limited data on energy transfers between aquatic food resources and larvae and between metamorphosed larvae and adjacent habitats preclude an accurate assessment of their roles as links between aquatic and terrestrial food webs.
2. During 2003–04, we derived prey-specific assimilation efficiencies, analysed stomach contents, and intensively sampled ambystomatid salamander assemblages in four ponds to quantify the trophic basis of larval production. Using estimates of the contribution of each prey taxon to larval production, we constructed quantitative food webs and assessed variation in pathways of energy flow associated with emergences.
3. Overall, metamorphosed salamanders exported 3–8% of total prey production, required to account for total salamander production, to adjacent forest. Aquatic insects, zooplankton and amphibian prey were most important to energy flow associated with emergence; amounts of larval production attributed to each of these prey types shifted during development and varied among salamander taxa.
4. The majority of variation in the trophic basis of production among species was attributed to copepods (Cyclopidae) and three families of aquatic insects (Chironomidae, Chaoboridae and Culicidae). Dominant prey types contributing to the production of metamorphosed salamanders varied among ponds, representing different pathways for energy transfers between aquatic resources and forest habitats. These findings further our understanding of the ecological roles of amphibians and thus the consequences of amphibian declines and extinctions.     

The limits of convergence in the collective behavior of competing marine taxa

Collective behaviors in biological systems such as coordinated movements have important ecological and evolutionary consequences. While many studies examine within‐species variation in collective behavior, explicit comparisons between functionally similar species from different taxonomic groups are rare. Therefore, a fundamental question remains: how do collective behaviors compare between taxa with morphological and physiological convergence, and how might this relate to functional ecology and niche partitioning? We examined the collective motion of two ecologically similar species from unrelated clades that have competed for pelagic predatory niches for over 500 million years—California market squid, Doryteuthis opalescens (Mollusca) and Pacific sardine, Sardinops sagax (Chordata). We (1) found similarities in how groups of individuals from each species collectively aligned, measured by angular deviation, the difference between individual orientation and average group heading. We also (2) show that conspecific attraction, which we approximated using nearest neighbor distance, was greater in sardine than squid. Finally, we (3) found that individuals of each species explicitly matched the orientation of groupmates, but that these matching responses were less rapid in squid than sardine. Based on these results, we hypothesize that information sharing is a comparably important function of social grouping for both taxa. On the other hand, some capabilities, including hydrodynamically conferred energy savings and defense against predators, could stem from taxon‐specific biology.     

Shifting of the life cycle and life-history traits of the fall webworm in relation to climate change

The effects of global warming on the life cycle and life‐history traits of the fall webworm, Hyphantria cunea (Drury) (Lepidoptera: Arctiidae), were investigated in Fukui, Japan. Our previous studies showed that the Fukui population had a predominantly bivoltine life cycle, but recently the life cycle has changed. In the present study, the life‐history traits of individuals collected in 2002 in Fukui were clarified and compared to those in the previous studies. The lower threshold temperature for development and the thermal constant for one generation were 10.6 °C and 724.4 degree days, respectively. Although these developmental parameters were not investigated in the previous studies, the difference of the developmental period between the present and previous results was negligible in the larval and pupal stages at 20 °C. The critical photoperiod for diapause induction was 14 h 29 min at 20 °C and 14 h 10 min at 25 °C. The critical photoperiod at 25 °C was shortened to 14 min from that of the previous studies for individuals collected in 1995. The incidence of pupal diapause in the second generation was investigated in individuals that were collected as fourth and fifth instars in the field. Some portion of individuals averted diapause even if they were kept under a short photoperiod of L14:D10 at 25 °C after collection. These results, together with climate data and field observations in Fukui, suggest that at least a part of the population has three generations per year at present. This shift of the life cycle occurred within 7 years and is probably related to global warming in recent years.     

More than meets the eye: detecting cryptic microgeographic population structure in a parasite with a complex life cycle

Nonrandom recruitment of parasites among hosts can lead to genetic differentiation among hosts and mating dynamics that promote inbreeding. It has been hypothesized that strictly aquatic parasites with intermediate hosts will behave as panmictic populations among hosts because ample opportunity exists for random mixing of unrelated individuals during transmission to the definitive host. A previous allozyme study on the marine trematode Lecithochirium fusiforme did not support this hypothesis; in that, there was genetic differentiation among, and significant heterozygote deficiencies within, definitive hosts. We revisit this system and use microsatellites to obtain multilocus genotypes. Our goal was to determine whether cryptic subgroups and/or the presence of clones could account for the apparent deviation from 'panmixia'. We find strong evidence for cryptic subdivision (three genetic clusters) that causes the Wahlund effect and differentiation among definitive hosts. After accounting for these cryptic groups, we see panmictic genetic structure among definitive hosts that is consistent with the 'high mixing in aquatic habitats' hypothesis. We see evidence for cotransmission of clones in all three clusters, but this level of clonal structure did not have a major impact in causing deviations from Hardy-Weinberg equilibrium, and only affected genetic differentiation among hosts in one cluster. A cursory examination of the data may have led to incorrect conclusions about nonrandom transmission. However, it is obvious in this system that there is more than meets the eye in relation to the actual make-up of parasite populations. In general, the methods we employ will be useful for elucidating hidden patterns in other organisms where cryptic structure may be common (e.g. those with limited morphology or complex life histories).     

Contrasting trophic‐cascade effects driven by variation in morphology of the perches used by a larval damselfly

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Energy flow and subsidies associated with the complex life cycle of ambystomatid salamanders in ponds and adjacent forest in southern Illinois

Breeding adults and metamorphosing larval amphibians transfer energy between freshwater and terrestrial ecosystems during seasonal migrations and emergences, although rarely has this been quantified. We intensively sampled ambystomatid salamander assemblages (Ambystoma opacum,A. maculatum, and A. tigrinum) in five forested ponds in southern Illinois to quantify energy flow associated with egg deposition, larval production, and emergence of metamorphosed larvae. Oviposition by female salamanders added 7.0–761.4 g ash-free dry mass (AFDM) year⁻¹ to ponds (up to 5.5 g AFDM m⁻² year⁻¹). Larval production ranged from 0.4 to 7.4 g AFDM m⁻² year⁻¹ among populations in three ponds that did not dry during larval development, with as much as 7.9 g AFDM m⁻² year⁻¹ produced by an entire assemblage. Mean larval biomass during cohort production intervals in these three ponds ranged from 0.1 to 2.3 g AFDM m⁻² and annual P/B (production/biomass) ranged from 4 to 21 for individual taxa. Emergent biomass averaged 10% (range=2–35%) of larval production; larval mortality within ponds accounted for the difference. Hydroperiod and intraguild predation limited larval production in some ponds, but emerging metamorphs exported an average of 70.0±33.9 g AFDM year⁻¹ (range=21.0–135.2 g AFDM year⁻¹) from ponds to surrounding forest. For the three ponds where larvae survived to metamorphosis, salamander assemblages provided an average net flux of 349.5±140.8 g AFDM year⁻¹ into pond habitats. Among all ponds, net flux into ponds was highest for the largest pond and decreased for smaller ponds with higher perimeter to surface area ratios (r ² =0.94, P<0.05, n=5). These results are important in understanding the multiple functional roles of salamanders and the impact of amphibian population declines on ecosystems. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Developing a predictive model for the energy content of goat milk as the basis for a functional unit formulation to be used in the life cycle assessment of dairy goat production systems

Recent reports on livestock environmental impact based on life cycle assessment (LCA) did not fully consider the case of the dairy goat. Assignment of an environmental impact (e.g. global warming potential) to a specific product needs to be related to the appropriate ‘unitary amount’ or functional unit (FU). For milk, the energy content may provide a common basis for a definition of the FU. To date, no ad hoc formulations for the FU of goat milk have been proposed. For these reasons, this study aimed to develop and test one or more predictive models (DPMs) for the gross energy (GE) content of goat milk, based on published compositional data, such as fat (F), protein, total solids (TS), solid non-fat matter (SNF), lactose (Lac) and ash. The DPMs were developed, selected and tested using a linear regression approach, as a meta-analysis (i.e. meta-regression) was not applicable. However, in the final stage, a control procedure for spurious findings was carried out using a Monte Carlo permutation test. Because several published predictive models (PPMs) for GE in cow milk and goat milk were found in the literature, they were tested on the same data set with which the DPMs were developed. The best-performing DPMs and PPMs were compared directly with a subset of the individual data retrieved from the literature. Overall, the paucity of direct measurements of the GE in goat milk was a limiting factor in collecting data from the literature; thus, only a small data set (n=26) was established, even though it was considered sufficiently representative of milks from different goat breeds. The three best PPMs based on F alone gave more biased estimates of the GE content of the goat milk than the three new DPMs based on F, F and SNF and F and TS, respectively. Accordingly, three different formulations of FU are proposed, depending on the availability of data including both F and TS (or F and SNF) or F alone. Even though several metrics can be used in defining the FU for milk to be used in LCAs of goat farming systems, the proposed FU formulations should be adopted in place of the similar energy-based ones developed for other dairy species.     

Predicting the population dynamics of the house dust mite Dermatophagoides pteronyssinus (Acari: Pyroglyphidae) in response to a constant hygrothermal environment using a model of the mite life cycle

A generalised model of the life cycle of a house dust mite, which can be tailored to any particular species of domestic mite, is presented. The model takes into account the effects of hygrothermal conditions on each life cycle phase. It is used in a computer simulation program, called POPMITE, which, by incorporating a population age structure, is able to predict population dynamics. The POPMITE simulation is adapted to the Dermatophagoides pteronyssinus (Acari: Pyroglyphidae) (DP) mite using published data on the egg development period, total development period, adult longevity, mortality during egg development, mortality during juvenile development, and fecundity of individual DP mites held at a range of constant hygrothermal conditions. An example is given which illustrates how the model functions under constant hygrothermal conditions. A preliminary validation of POPMITE is made by a comparison of the POPMITE predictions with published measurements of population growth of DP mites held at a range constant hygrothermal conditions for 21 days. The POPMITE simulation is used to provide predictions of population growth or decline for a wide range of constant relative humidity and temperature combinations for 30 and 60 days. The adaptation of the model to correctly take account of fluctuating hygrothermal conditions is discussed.