Does a complex life cycle affect adaptation to environmental change? Genome-informed insights for characterizing selection across complex life cycle

Complex life cycles, in which discrete life stages of the same organism differ in form or function and often occupy different ecological niches, are common in nature. Because stages share the same genome, selective effects on one stage may have cascading consequences through the entire life cycle. Theoretical and empirical studies have not yet generated clear predictions about how life cycle complexity will influence patterns of adaptation in response to rapidly changing environments or tested theoretical predictions for fitness trade-offs (or lack thereof) across life stages. We discuss complex life cycle evolution and outline three hypotheses—ontogenetic decoupling, antagonistic ontogenetic pleiotropy and synergistic ontogenetic pleiotropy—for how selection may operate on organisms with complex life cycles. We suggest a within-generation experimental design that promises significant insight into composite selection across life cycle stages. As part of this design, we conducted simulations to determine the power needed to detect selection across a life cycle using a population genetic framework. This analysis demonstrated that recently published studies reporting within-generation selection were underpowered to detect small allele frequency changes (approx. 0.1). The power analysis indicates challenging but attainable sampling requirements for many systems, though plants and marine invertebrates with high fecundity are excellent systems for exploring how organisms with complex life cycles may adapt to climate change.

Sexual Development in Non-Human Parasitic Apicomplexa: Just Biology or Targets for Control?

The phylum Apicomplexa is a major group of protozoan parasites including gregarines, coccidia, haemogregarines, haemosporidia and piroplasms, with more than 6000 named species. Three of these subgroups, the coccidia, hemosporidia, and piroplasms, contain parasites that cause important diseases of humans and animals worldwide. All of them have complex life cycles involving a switch between asexual and sexual reproduction, which is key to their development. Fertilization (i.e., fusion of female and male cells) results in the formation of a zygote that undergoes meiosis, forming a new generation of asexual stages. In eukaryotes, sexual reproduction is the predominant mode of recombination and segregation of DNA. Sex is well documented in many protist groups, and together with meiosis, is frequently linked with transmission to new hosts. Apicomplexan sexual stages constitute a bottleneck in the life cycle of these parasites, as they are obligatory for the development of new transmissible stages. Consequently, the sexual stages represent attractive targets for vaccination. Detailed understanding of apicomplexan sexual biology will pave the way for the design and implementation of effective transmission-blocking strategies for parasite control. This article reviews the current knowledge on the sexual development of Apicomplexa and the progress in transmission-blocking vaccines for their control, their advantages and limitations and outstanding questions for the future.

Transitional genomes and nutritional role reversals identified for dual symbionts of adelgids (Aphidoidea: Adelgidae)

Many plant-sap-feeding insects have maintained a single, obligate, nutritional symbiont over the long history of their lineage. This senior symbiont may be joined by one or more junior symbionts that compensate for gaps in function incurred through genome-degradative forces. Adelgids are sap-sucking insects that feed solely on conifer trees and follow complex life cycles in which the diet fluctuates in nutrient levels. Adelgids are unusual in that both senior and junior symbionts appear to have been replaced repeatedly over their evolutionary history. Genomes can provide clues to understanding symbiont replacements, but only the dual symbionts of hemlock adelgids have been examined thus far. Here, we sequence and compare genomes of four additional dual-symbiont pairs in adelgids. We show that these symbionts are nutritional partners originating from diverse bacterial lineages and exhibiting wide variation in general genome characteristics. Although dual symbionts cooperate to produce nutrients, the balance of contributions varies widely across pairs, and total genome contents reflect a range of ages and degrees of degradation. Most symbionts appear to be in transitional states of genome reduction. Our findings support a hypothesis of periodic symbiont turnover driven by fluctuating selection for nutritional provisioning related to gains and losses of complex life cycles in their hosts.

Field variations in mass at metamorphosis in a stream frog, Odorrana splendida, and their relationship with the stream environment

Animals with complex life cycles, such as amphibians, shift their habitats when they metamorphose. Metamorphosing traits (e.g., size at, and timing of, metamorphosis) at an early stage can affect the growth, reproduction, and survival in the adult stage. Thus, metamorphosing traits are important factors that affect the fitness of the individuals. Although size at metamorphosis in the field has been investigated in amphibians, its relationship with environmental factors has been scarce. We aimed to quantify variations in the mass at metamorphosis of a stream frog, Odorrana splendida, among multiple streams, and show the relationship of these variations with environmental conditions. We searched for metamorphs in 11 field streams and measured their body size. We then examined the relationship between environmental conditions of each stream and the mass at metamorphosis to reveal the factors determining the mass. We found 229 metamorphs over three years. The estimated mass at metamorphosis ranged from 0.17 g to 1.44 g, with a coefficient of variation among streams of 0.38. The size at metamorphosis significantly differed among streams, and was found to be positively affected by water temperature and chlorophyll a concentration, and negatively affected by altitude, slope gradient, and the number of adult calls. We showed that O. splendida has a large variation in mass at metamorphosis within and among natural streams. A lower mass at metamorphosis may correlate with scarce food resources in the stream and higher competition during the larval stages, resulting from a higher number of mating adults.

Promising Technologies in the Field of Helminth Vaccines

Helminths contribute a larger global burden of disease than both malaria and tuberculosis. These eukaryotes have caused human infections since before our earliest recorded history (i.e.: earlier than 1200 B.C. for Schistosoma spp.). Despite the prevalence and importance of these infections, helminths are considered a neglected tropical disease for which there are no vaccines approved for human use. Similar to other parasites, helminths are complex organisms which employ a plethora of features such as: complex life cycles, chronic infections, and antigenic mimicry to name a few, making them difficult to target by conventional vaccine strategies. With novel vaccine strategies such as viral vectors and genetic elements, numerous constructs are being defined for a wide range of helminth parasites; however, it has yet to be discussed which of these approaches may be the most effective. With human trials being conducted, and a pipeline of potential anti-helminthic antigens, greater understanding of helminth vaccine-induced immunity is necessary for the development of potent vaccine platforms and their optimal design. This review outlines the conventional and the most promising approaches in clinical and preclinical helminth vaccinology.

From Insects to Frogs, Egg–Juvenile Recruitment Can have Persistent Effects on Population Sizes

Understanding what regulates population sizes of organisms with complex life cycles is challenging because limits on population sizes can occur at any stage or transition. We extend a conceptual framework to explore whether numbers of successfully laid eggs determine densities of later stages in insects, fish, amphibians, and snails inhabiting marine, freshwater, or terrestrial habitats. Our review suggests novel hypotheses, which propose characteristics of species or environments that create spatial variation in egg densities and predict when such patterns are maintained throughout subsequent life-cycle stages. Existing data, although limited, suggest that persistent, strong associations between egg and subsequent juvenile densities are likely for species where suitable egg-laying habitat is in short supply. Those associations are weakened in some environments and for some species by density-dependent losses of eggs or hatchlings. Such cross-ecosystem comparisons are fundamental to generality in ecology but demand place-based understandings of species’ biology and natural history. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

The diversity and natural history of parasites

Parasites are more numerous than non-parasitic species and have evolved in virtually all groups of organisms, such as viruses, prokaryotes (bacteria), protozoa, fungi, nematodes, flatworms, acantocephalans, annelids, crustaceans, and arthropods (crustacea, mites, ticks, insects). These groups have adapted to the parasitic lifestyle in very many ways. Evolution towards parasitism has also followed different routes. Initial steps such as phoresy, followed by later consumption of the transport host, are plausible evolutionary routes. Alternatively, formerly free-living forms have become commensals before evolving parasitism. Complex life cycles with several hosts evolved by scenarios such as upward (adding a new host upwards in the food chain), downward, or lateral incorporation, driven by the advantage of extending growth phases within hosts and increasing fecundity. Examples are digenea; other parasites have added vectors to their life cycle.

Dynamic methylation of histone H3K18 in differentiating Theileria parasites

Lysine methylation on histone tails impacts genome regulation and cell fate determination in many developmental processes. Apicomplexa intracellular parasites cause major diseases and they have developed complex life cycles with fine-tuned differentiation events. Yet, apicomplexa genomes have few transcription factors and little is known about their epigenetic control systems. Tick-borne Theileria apicomplexa species have relatively small, compact genomes and a remarkable ability to transform leucocytes in their bovine hosts. Here we report enriched H3 lysine 18 monomethylation (H3K18me1) on the gene bodies of repressed genes in Theileria macroschizonts. Differentiation to merozoites (merogony) leads to decreased H3K18me1 in parasite nuclei. Pharmacological manipulation of H3K18 acetylation or methylation impacted parasite differentiation and expression of stage-specific genes. Finally, we identify a parasite SET-domain methyltransferase (TaSETup1) that can methylate H3K18 and represses gene expression. Thus, H3K18me1 emerges as an important epigenetic mark which controls gene expression and stage differentiation in Theileria parasites.

Trematode parasite cercariae as food in model freshwater trophic interactions

Free-living parasite stages are important but often overlooked components of ecosystems, especially their role(s) in food webs. Trematode parasites have complex life cycles that include a motile transmission phase, cercariae, that are produced in great quantities within aquatic snail hosts and join the zooplankton community after emerging. Here I examined how cercariae presence affected the population abundance of a common freshwater zooplanktonic animal (Daphnia) when predators were present. I also sought to determine the pathways taken by cercariae-derived carbon within a model freshwater food web by using the stable isotope 13C as a tracer. I found that Daphnia population abundance positively benefitted from cercariae presence when larval dragonfly predators were present, serving as alternate prey. I also found that 13C was an effective tool to track the flow of cercarial carbon, demonstrating high consumption by benthic consumers, as well as the utility of this method for use in future studies.