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Biology subjects

Aardema, M. L.

Publications and source records attributed to Aardema, M. L..

8 recordsLinked to original sources

Cis-regulatory evolution of Wnt-family genes contributes to a morphological difference between silkworm species.

Closely related species often exhibit distinct morphologies that can contribute to species-specific adaptations and reproductive isolation. One example are Lepidopteran caterpillar appendages, such as the "caudal horn" of Bombycoidea moths, which have evolved substantial morphological diversity among species in this group. Using interspecific crosses, we identify the genetic basis of the caudal horn size difference between Bombyx mori and its closest relative B. mandarina. The three largest of eight QTL account for one third the mean horn length difference between the species. The largest of these, on chromosome 4, encompasses a conserved Wnt family gene cluster, key upstream regulators that are well-known for their roles in morphological diversification in animals. Using allele-specific expression analysis and CRISPR/Cas9 knockouts, we show that tissue-specific cis-regulatory changes to Wnt1 and Wnt6 contribute to the species difference in caudal horn size. This kind of modularity enables highly pleiotropic genes, including key upstream growth regulators, to contribute to the evolution of morphological traits without causing widespread deleterious effects. SignificanceThis study explores the genetic basis of a distinct morphological trait that varies between two closely related moth species, providing insights into the evolution of morphological diversity. By identifying cis-regulatory changes in two Wnt family genes as major contributors, this work underscores the importance of developmental gene regulatory networks in shaping species-specific traits. The findings illustrate how even small modifications in major upstream regulator genes can drive significant phenotypic variation, revealing how genetic changes in key growth regulators fuel the diversification of form and function. These results advance our understanding of the mechanisms behind the evolution of complex morphological traits.

evolutionary biology↗

Ancient origin of an urban underground mosquito

Understanding how life is adapting to urban environments represents an important challenge in evolutionary biology. Here we investigate a widely cited example of urban adaptation, Culex pipiens form molestus, also known as the London Underground Mosquito. Population genomic analysis of [~]350 contemporary and historical samples counter the popular hypothesis that molestus originated belowground in London less than 200 years ago. Instead, we show that molestus first adapted to human environments aboveground in the Middle East over the course of >1000 years, likely in concert with the rise of agricultural civilizations. Our results highlight the role of early human society in priming taxa for contemporary urban evolution and have important implications for understanding arbovirus transmission.

evolutionary biology↗

The genomic and cellular basis of biosynthetic innovation in rove beetles

How evolution at the cellular level potentiates change at the macroevolutionary level is a major question in evolutionary biology. With >66,000 described species, rove beetles (Staphylinidae) comprise the largest metazoan family. Their exceptional radiation has been coupled to pervasive biosynthetic innovation whereby numerous lineages bear defensive glands with diverse chemistries. Here, we combine comparative genomic and single-cell transcriptomic data from across the largest rove beetle clade, Aleocharinae. We retrace the functional evolution of two novel secretory cell types that together comprise the tergal gland--a putative catalyst behind Aleocharinaes megadiversity. We identify key genomic contingencies that were critical to the assembly of each cell type and their organ-level partnership in manufacturing the beetles defensive secretion. This process hinged on evolving a mechanism for regulated production of noxious benzoquinones that appears convergent with plant toxin release systems, and synthesis of an effective benzoquinone solvent that weaponized the total secretion. We show that this cooperative biosynthetic system arose at the Jurassic-Cretaceous boundary, and that following its establishment, both cell types underwent [~]150 million years of stasis, their chemistry and core molecular architecture maintained almost clade-wide as Aleocharinae radiated globally into tens of thousands of lineages. Despite this deep conservation, we show that the two cell types have acted as substrates for the emergence of adaptive, biochemical novelties--most dramatically in symbiotic lineages that have infiltrated social insect colonies and produce host behavior-manipulating secretions. Our findings uncover genomic and cell type evolutionary processes underlying the origin, functional conservation and evolvability of a chemical innovation in beetles.

evolutionary biology↗

The path to "femmes fatales": the evolution of toxin resistance in predatory fireflies.

Toxic cardiotonic steroids (CTS) act as a defense mechanism in many firefly species (Lampyridae) by inhibiting a crucial enzyme called Na+,K+-ATPase (NKA). While most fireflies produce these toxins internally, species of the genus Photuris acquire them from a surprising source: predation on other fireflies. The contrasting physiology of toxin exposure and sequestration between Photuris and other firefly genera suggests that distinct strategies may be required to prevent self-intoxication. Our study demonstrates that both Photuris and their firefly prey have evolved highly-resistant NKAs. Using an evolutionary analysis of the specific target of CTS (ATP) in fireflies, and gene-editing in Drosophila, we find that the initial steps towards resistance were shared among Photuris and other firefly lineages. However, the Photuris lineage subsequently underwent multiple rounds of gene duplication and neofunctionalization, resulting in the development of ATP paralogs that are differentially expressed and exhibit increasing resistance to CTS. In contrast, other firefly species have maintained a single copy. Our results implicate gene duplication as a facilitator in the transition of Photuris to its distinct ecological role as predator of toxic firefly prey. One-Sentence SummaryGene duplication and neofunctionalization distinguish firefly predators from their toxic firefly prey.

evolutionary biology↗

Demographic expansions and the emergence of host specialization in genetically distinct strains of the tick-transmitted bacterium Anaplasma phagocytophilum

Bacteria species that must obligately replicate in vertebrate host cells make up a large proportion of the prokaryotic pathogens with human and veterinary health implications. In such bacterial taxa, extrinsic processes play an important role in influencing the phylogenetic diversity of viable hosts ( host range). These processes include both changes in host population densities and shifts in host geographic distributions. In Europe, distinct genetic strains of the tick-vectored bacterium Anaplasma phagocytophilum circulate among mammals in three discrete enzootic cycles. To date, the factors that contributed to the emergence of these strains have been poorly studied. Here we show that the strain which predominately infects roe deer (Capreolus capreolus) is evolutionarily derived. Its divergence from a likely host-generalist ancestor occurred after the last glacial maximum as mammal populations, including roe deer, recolonized the European mainland from southern refugia. We also provide evidence that this host-specialist strains effective population size (Ne) has tracked changes in the population of its roe deer host. Specifically, both host and bacterium appear to have undergone substantial increases in Ne over the past 1,500 years. In contrast, we show that while it appears to have undergone a major population expansion starting [~]3,500 years ago, in the past 500 years the contemporary host-generalist strain has experienced a substantial reduction in genetic diversity levels, possible as the result of reduced transmission opportunities between competent hosts. IMPORTANCEThe findings of this study are some of the first to examine specific events in the evolution of host specialization in a naturally occurring, obligately intracellular bacterial species. They show that host range shifts and the emergence of host specialization may occur during periods of population growth in a host-generalist ancestor. The results discussed here also show the close correlation between demographic patterns in host and pathogen for a specialist system. These findings have important relevance for our understanding of the evolution of host-range diversity. They may inform future work on host-range dynamics and provide insights for understanding the emergence of pathogens which have human and veterinary health implications.

evolutionary biology↗

A gene-based capture assay for surveying patterns of genetic diversity and insecticide resistance in a worldwide group of invasive mosquitoes

Understanding patterns of diversification, genetic exchange, and pesticide resistance in insect species of human health concern is necessary for effective population reduction and management. With the broad availability of next-generation sequencing technologies, one of the best approaches for surveying such patterns involves the simultaneous genotyping of many samples for large numbers of genetic markers from across the known genome. To this end, the targeting of gene sequences of known function or inheritance can be a cost-effective strategy. One insect group of substantial health concern are the mosquito taxa that make up the Culex pipiens complex. Members of this complex transmit damaging arboviruses and filariae worms to humans, as well as other pathogens that are detrimental to endangered vertebrate species such as bird malaria. Here we describe our development of a targeted gene-based assay for surveying genetic diversity and population structure in this mosquito complex. To test the utility of this assay, we examined taxonomic divergence among samples from several members of the complex, as well as distinct populations of the relatively under-studied Culex quinquefasciatus, an urban pantropical species. We also examined the presence of known insecticide-resistance conferring alleles. Broadly, our developed gene-based assay proved effective for examining patterns of taxonomic and geographic clustering within the species complex, as well as for surveying genetic variants that have been associated with insecticide resistance. This assay will be useful for future studies that aim to understand the genetic mechanisms underlying the evolution of ubiquitous and increasingly damaging disease vectors.

genomics↗

Persistence and expansion of cryptic endangered red wolf genomic ancestry along the American Gulf coast

Admixture and introgression play a critical role in adaptation and genetic rescue that has only recently gained a deeper appreciation. Here, we explored the geographic and genomic landscape of cryptic ancestry of the endangered red wolf that persists within the genome of a ubiquitous sister taxon, the coyote, all the while the red wolf has been extinct in the wild since the early 1980s. We assessed admixture across 102,621 SNP loci genotyped in 293 canid genomes. We found support for increased red wolf ancestry along an east-to-west gradient across the southern United States that was associated with historical admixture in the past 100 years. Southwestern Louisiana and southeastern Texas, the geographic zone where the last red wolves were known prior to their extinction in the wild, contained the highest and oldest levels of red wolf ancestry. X-linked regions of low recombination rates were depleted of introgression, relative to the autosomes, suggestive of the large X effect and enrichment with loci involved in maintaining reproductive isolation. Recombination rate was positively correlated with red wolf ancestry across coyote genomes, consistent with theoretical predictions. The geographic and genomic extent of cryptic red wolf ancestry can provide novel and variable genomic resources for the survival of the endangered red wolf.

evolutionary biology↗

The urban-adapted underground mosquito, Culex molestus, maintains exogenously influenced circadian rhythms despite an absence of photoperiodically induced dormancy

In temperate climates, the mosquito Culex molestus lives almost exclusively in urban underground locations such as flooded basements, sewer systems and subway tunnels. Unlike most other mosquito taxa found at higher latitudes, Cx. molestus remains active and continues to breed throughout the winter. This is attributable to year-round above freezing temperatures in its preferred underground habitats combined with an inability to enter a state of arrested development ( diapause) in response to shortening photoperiods in autumn. Prior studies have shown that the genes associated with circadian rhythms (i.e. clock genes) also influence the photoperiodic induction of diapause in the closely related mosquito, Cx. pipiens. These results suggest that molecular changes in one or more clock genes could contribute to the absence of photoperiodically induced diapause in Cx. molestus. As Cx. molestus predominantly inhabits underground locations generally devoid of a predictable photoperiod, such mutations may not be removed by purifying selection as they would have minimal fitness consequences. To examine the possibility that Cx. molestus- specific genetic changes in one or more clock genes correlate with its inability to enter a photoperiodically induced dormant state, we first used genomic data to search for inactivating mutations or other structural variants in genes known to influence circadian rhythms in Diptera ( flies). We further investigated non-synonymous, derived genetic divergence in this same class of genes. Next, we generated transcriptome data from multiple life-stages of Cx. molestus to survey binary expression of annotated clock genes throughout this mosquitos lifecycle. Finally, we carried out experimental studies to assess the extent to which Cx. molestus retains exogenously influenced circadian rhythms, and whether it harbors any tendencies towards dormancy when exposed to a shortened photoperiod. Our results indicate that the gene Helicase domino (dom) has a nine-nucleotide, in-frame deletion specific to Cx. molestus. Previous work has shown that splice variants in this gene influence circadian behavior in Drosophila melanogaster. We also find derived, non-synonymous single nucleotide polymorphisms (SNPs) in eight genes that may also affect circadian rhythms and/or diapause induction in Cx. molestus. Four other circadian genes were found to have no quantifiable expression during any examined life stage, suggesting potential regulatory variation. Our experimental results confirm that Cx. molestus retains exogenously-influenced circadian rhythms but is not induced to enter a dormant state by a shortened photoperiod. Collectively, these findings show that the distinct, but potentially molecularly interconnected life-history traits of diapause induction and circadian rhythms are decoupled in Cx. molestus and suggest that this taxon may be a valuable tool for exploring exogenously influenced phenotypes in mosquitoes more broadly.

evolutionary biology↗