For insects that exhibit wing polyphenic development, abiotic and biotic signals dictate the adult wing morphology of the insect in an adaptive manner such that in stressful environments the formation of a flight-capable morph is favored and in low-stress environments, a flightless morph is favored. While there is a relatively large amount known about the environmental cues that dictate morph formation in wing polyphenic hemipterans like planthoppers and aphids, whether those cues dictate the same morphs in non-hemipteran (i.e., cricket) wing polyphenic species has not been explicitly investigated. To experimentally test the generality of environmental cue determination of wing polyphenism across taxa with diverse life histories, in this study, we tested the importance of food quantity, parasitic infection, and tactile cues on wing morph determination in the wing polyphenic sand field cricket, Gryllus firmus. Our results also show that certain stress cues, such as severe diet quantity limitation and parasitic infection, actually led to an increase in the production of flightless morph. Based on these findings, our results suggest that physiological and genetic constraints are important to an organism’s ability to respond to environmental variation in an adaptive manner beyond simple life history trade-offs.
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Abstract Sexually selected weapons, such as the antlers of deer, claws of crabs, and tusks of beaked whales, are strikingly diverse across taxa and even within groups of closely related species. Phylogenetic comparative studies have typically taken a simplified approach to investigate the evolution of weapon diversity, examining the gains and losses of entire weapons, major shifts in size or type, or changes in location. Less understood is how individual weapon components evolve and assemble into a complete weapon. We addressed this question by examining weapon evolution in the diverse, multi-component hind-leg and body weapons of leaf-footed bugs, superfamily Coreoidea (Hemiptera: Heteroptera). Male leaf-footed bugs use their morphological weapons to fight for access to mating territories. We used a large multilocus dataset comprised of ultraconserved element loci for 248 species and inferred evolutionary transitions among component states using ancestral state estimation. Our results suggest that weapons added components over time with some evidence of a cyclical evolutionary pattern—gains of components followed by losses and then gains again. Furthermore, our best estimate indicated that certain trait combinations evolved repeatedly across the phylogeny, suggesting that they function together in battle or that they are genetically correlated. This work reveals the remarkable and dynamic evolution of weapon form in the leaf-footed bugs and provides insights into weapon assembly and disassembly over evolutionary time.
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Abstract Dietary macronutrients regulate life span and aging, yet little is known about their evolutionary effects. Here, we examine the evolutionary response of these traits in decorated crickets (Gryllodes sigillatus) maintained on diets varying in caloric content and protein-to-carbohydrate ratio. After 37 generations, each population was split: half remained on the evolution diet, and half switched to a standardized diet. Crickets lived longer and aged slower when evolving on high-calorie (both sexes) and carbohydrate-biased (females only) diets and had lower baseline mortality on high-calorie (females only) diets. However, on the standardized diet, crickets lived longer when evolving on high-calorie diets (both sexes), aged slower on high-calorie (females only) and carbohydrate-biased (both sexes) diets, and had lower baseline mortality on high-calorie (males only) and protein-biased (both sexes) diets. Life span was longer, and baseline mortality was lower when provided with the evolution vs. the standardized diet, but the aging rate was comparable. Moreover, life span was longer, aging slower (females only), and baseline mortality was lower (males only) compared to our evolved baseline, suggesting varying degrees of dietary adaptation. Collectively, we show dietary components influence the evolution of life span and aging in different ways and highlight the value of combining experimental evolution with nutritional geometry.
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Abstract The origin of life remains one of the greatest enigmas in science. The immense leap in complexity between prebiotic soup and cellular life challenges historically “chemistry-forward” and “biology-backwards” approaches. Evolution must have bridged this gap in complexity, so understanding factors that influence evolutionary outcomes is critical for exploring life’s emergence. Here, we review insights from ecology and evolution and their application throughout abiogenesis. In particular, we discuss how ecological and evolutionary constraints shape the evolution of biological innovation. We propose an “eco-evolutionary” approach, which is agnostic towards particular chemistries or environments and instead explores the several ways that an evolvable system may emerge and gain complexity.
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Abstract A major predicted constraint on the evolution of anti-herbivore defense in plants is the nonindependent expression of traits mediating resistance. Since herbivore attack can be highly variable across plant tissues, we hypothesized that correlations in toxin expression within and between plant tissues may limit population differentiation and, thus, plant adaptation. Using full-sib families from two nearby (<1 km) common milkweed (Asclepias syriaca) populations, we investigated genetic correlations among 28 distinct cardenolide toxins within and between roots, leaves, and seeds and examined signatures of tissue-specific divergent selection between populations by QST–FST comparisons. The prevalence, direction, and strength of genetic correlations among cardenolides were tissue specific, and concentrations of individual cardenolides were moderately correlated between tissues; nonetheless, the direction and strength of correlations were population specific. Population divergence in the cardenolide chemistry was stronger in roots than in leaves and seeds. Divergent selection on individual cardenolides was tissue and toxin specific, except for a single highly toxic cardenolide (labriformin), that showed divergent selection across all plant tissues. Heterogeneous evolution of cardenolides within and between tissues across populations appears possible due to their highly independent expression. This independence may be common in nature, especially in specialized interactions in which distinct herbivores feed on different plant tissues.
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Abstract Our understanding of the evolutionary significance of ectoparasites in natural communities is limited by a paucity of information concerning the mechanisms and heritability of resistance to this ubiquitous group of organisms. Here, we report the results of artificial selection for increasing ectoparasite resistance in replicate lines of Drosophila melanogaster derived from a field-fresh population. Resistance, as ability to avoid infestation by naturally co-occurring Gamasodes queenslandicus mites, increased significantly in response to selection and realized heritability (SE) was estimated to be 0.11 (0.0090). Deployment of energetically expensive bursts of flight from the substrate was a main mechanism of host resistance that responded to selection, aligning with previously documented metabolic costs of fly behavioral defenses. Host body size, which affects parasitism rate in some fly–mite systems, was not shifted by selection. In contrast, resistant lines expressed significant reductions in larva-to-adult survivorship with increasing toxic (ammonia) stress, identifying an environmentally modulated preadult cost of resistance. Flies selected for resistance to G. queenslandicus were also more resistant to a different mite, Macrocheles subbadius, suggesting that we documented genetic variation and a pleiotropic cost of broad-spectrum behavioral immunity against ectoparasites. The results demonstrate significant evolutionary potential of resistance to an ecologically important class of parasites.
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Abstract Allopolyploids represent a new frontier in species discovery among embryophytes. Within mosses, allopolyploid discovery is challenged by low morphological complexity. The rapid expansion of sequencing approaches in addition to computational developments to identifying genome merger and whole-genome duplication using variation among nuclear loci representing homeologs has allowed for increased allopolyploid discovery among mosses. Here, we test a novel approach to phasing homeologs within loci and phasing loci across subgenomes, or subgenome assignment, called Homologizer, in the family Funariaceae. We confirm the intergeneric hybrid nature of Entosthodon hungaricus, and the allopolyploid origin of Physcomitrium eurystomum and one population of Physcomitrium collenchymatum. We also reveal that hybridization gave rise to Physcomitrium immersum, as well as to yet unrecognized lineages sharing the phenotype of Physcomitrium pyriforme and Physcomitrium sphaericum. Our findings demonstrate the utility of our approach when working with polyploid genomes, and its value in identifying progenitor species using target capture data.
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Abstract Asexual reproduction is ancestral in prokaryotes; the switch to sexuality in eukaryotes is one of the major transitions in the history of life. The study of the maintenance of sex in eukaryotes has raised considerable interest for decades and is still one of evolutionary biology’s most prominent question. The observation that many asexual species are of hybrid origin has led some to propose that asexuality in hybrids results from sexual processes being disturbed because of incompatibilities between the two parental species’ genomes. However, in some cases, failure to produce asexual F1s in the lab may indicate that this mechanism is not the only road to asexuality in hybrid species. Here, we present a mathematical model and propose an alternative, adaptive route for the evolution of asexuality from previously sexual hybrids. Under some reproductive alterations, we show that asexuality can evolve to rescue hybrids’ reproduction. Importantly, we highlight that when incompatibilities only affect the fusion of sperm and egg’s genomes, the two traits that characterize asexuality, namely unreduced meiosis and the initiation of embryogenesis without the incorporation of the sperm’s pronucleus, can evolve separately, greatly facilitating the overall evolutionary route. Taken together, our results provide an alternative, potentially complementary explanation for the link between asexuality and hybridization.
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Abstract The enormous population sizes and wide biogeographical distribution of many microbial eukaryotes set the expectation of high levels of intraspecific genetic variation. However, studies investigating protist populations remain scarce, mostly due to limited ‘omics data. Instead, most genetics studies of microeukaryotes have thus far relied on single loci, which can be misleading and do not easily allow for detection of recombination, a hallmark of sexual reproduction. Here, we analyze >40 genes from 72 single-cell transcriptomes from two morphospecies—Hyalosphenia papilio and Hyalosphenia elegans—of testate amoebae (Arcellinida, Amoebozoa) to assess genetic diversity in samples collected over four years from New England bogs. We confirm the existence of cryptic species based on our multilocus dataset, which provides evidence of recombination within and high levels of divergence between the cryptic species. At the same time, total levels of genetic diversity within cryptic species are low, suggesting that these abundant organisms have small effective population sizes, perhaps due to extinction and repopulation events coupled with efficient modes of dispersal. This study is one of the first to investigate population genetics in uncultivable heterotrophic protists using transcriptomics data and contributes towards understanding cryptic species of nonmodel microeukaryotes.