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Lo, N.

Publications and source records attributed to Lo, N..

At least 19 recordsLinked to original sources

The ancestral endosymbiont Blattabacterium was lost ten times independently in Blattellidae, Pseudophyllodromiidae and Anaplectidae cockroaches

Most cockroaches and the termite Mastotermes darwiniensis are associated with Blattabacterium, an ancient obligate endosymbiont that participates in the nitrogen metabolism of its host. Blattabacterium has been vertically transmitted since it was acquired by the common ancestor of cockroaches and termites and was reportedly lost twice, once in the cockroach genus Nocticola and once in all termites except Mastotermes darwiniensis. Here, we acquired cockroach specimens spanning most of the cockroach phylogenetic tree to study Blattabacterium using shotgun sequencing. We found no traces of Blattabacterium in 64 specimens from ten independent lineages of cockroaches across three families: Blattellidae, Pseudophyllodromiidae, and Anaplectidae. The absence of Blattabacterium was confirmed with three PCR amplifications targeting the 16S and 23S ribosomal genes with primers specific to Blattabacterium. Notably, cockroaches lacking Blattabacterium were often infected by Rickettsia and Wolbachia, many of which were related to the mutualistic Wolbachia strain of Cimex lectularius, the common bed bug. These results indicate that cockroaches from Blattellidae, Pseudophyllodromiidae and Anaplectidae have lost their ancestral Blattabacterium endosymbiont at least ten times independently, with many of these losses possibly facilitated and compensated by new associations with mutualistic Wolbachia strains that may help provision the host with B vitamins.

evolutionary biology↗

Characterisation and genomic analysis of bacterial nutritional endosymbionts in Australian ticks from shotgun metagenomic sequencing

Ticks are obligate hematophagous arthropods and feed exclusively on blood. As blood is nutrient-poor, ticks rely on bacterial endosymbionts to synthesise nutrients, yet the diversity and functional roles of these symbionts in Australian ticks remain largely uncharacterised. This is critical to address as these ticks are of high medical importance in Australia. In this study, shotgun metagenomic sequencing was performed on Bothriocroton concolor, Bothriocroton hydrosauri, Haemaphysalis longicornis and Ixodes holocyclus, enabling the recovery of six complete or partial metagenome-assembled genomes (MAGs). These comprised Coxiella-like endosymbionts (CLE), a facultative Rickettsia symbiont, and two Midichloria mitochondrii strains (Ixholo1 and Ixholo2). Functional annotation of these taxon-specific symbionts revealed the absence of virulence factors and the presence of B-vitamin and/or heme biosynthesis genes, indicative of nutritional mutualism, which is essential for tick hematophagy. The CLEs additionally harbour genes of the shikimate pathway, which modulate blood feeding in ticks by regulating serotonin biosynthesis. Furthermore, functional annotation and pangenomic analysis of Midichloria spp. found evidence that the genus may encompass multiple species, as well as the retention of genes potentially associated with an intramitochondrial lifestyle in M. mitochondrii Ixholo2. Tick microbiomes are dominated by non-pathogenic microorganisms, which are often overshadowed by pathogens. These include the endosymbionts, which can influence host biology and pathogen transmission, and are fundamental for the development of diagnostic tools and taxon-specific tick biocontrols.

microbiology↗

Diversification of pre-mating behaviors through temporal reordering of components

Many biological processes, including mating behavior, are structured as ordered sequences in which each step enables the next. Diversity of such processes usually arises through the addition or loss of components rather than through changes in their order, since reordering can disrupt functional integration. Here we show that reordering of the steps associated with termite nuptial pairing can generate behavioral diversity. In most termites, dispersed adults shed their wings before initiating tandem pairing, as wings interfere with communication between females and males. However, we found that in the Australian termite, Microcerotermes nervosus, tandem running occurs prior to wing shedding, and the act of tandem running itself facilitates dealation. Video tracking revealed that wing removal improves movement coordination, and comparative analysis of sympatric species showed that M. nervosus exhibits much higher tandem stability than others. These results suggest that enhanced movement coordination of this species may have potentiated step reordering. Our findings demonstrate that even functionally conserved sequences can be reorganized and that overcoming such constraints can open novel pathways for behavioral diversification.

animal behavior and cognition↗

Increases in invertebrate abundance and shifts in assemblage composition following Rodent Eradication on Lord Howe Island

Invasive species are one of the major threatening processes impacting biodiversity on islands. In particular, introduced rodents represent one of the most serious threats to island ecosystems, affecting a wide range of native plants, vertebrates and invertebrates. While nearly ubiquitous on human-modified islands, the last four decades have seen the advent of targeted rodent eradications, which have generally resulted in positive impacts for biodiversity. Invertebrates, which are crucial to the functioning of island ecosystems, are known to be negatively impacted by rodents, but their response to rodent removal is less well understood. The largest rodent eradication on an inhabited island was undertaken in 2019 on Australias Lord Howe Island, which successfully extirpated black rats (Rattus rattus) and house mice (Mus musculus) more than a century after their introduction. To examine the impacts of rodents on invertebrates on Lord Howe Island, we collected arboreal and terrestrial species both pre- and post-eradication and identified them to Order. Total invertebrate abundance increased after the eradication of rodents, alongside substantial shifts in assemblage composition, however Ordinal diversity did not change significantly. Orders with large increases in abundance included Isopoda and Blattodea, while the abundance of Coleoptera and Polydesmida did not change. In addition, the abundance of large invertebrates, which are presumably subject to stronger rat predation, rose dramatically following rodent eradication. Our results suggest an ecological rearrangement following the relaxation of predation pressure and augment documented evidence of improved biodiversity outcomes for forest tree species, seabirds and land birds.

ecology↗

Island syndrome in the critically endangered Lord Howe Island cockroach Panesthia lata

Following island colonisation, organisms experience a unique array of selective pressures, giving rise to a somewhat predictable suite of morphological, demographic and ecological adaptations known as the "island syndrome". Studies of the island syndrome have provided valuable insights into processes of speciation, community assembly, adaptive radiation and ecological release, alongside many others. However, to date, behavioural aspects of island adaptation have comparatively received little scientific attention, especially among invertebrates. In this study we examined the agonistic, courtship and aggregation behaviour of the endangered Lord Howe Island cockroach Panesthia lata, and compared these to its Australian sister species Panesthia cribrata. Behavioural assays revealed that while courtship behaviour was relatively stable across the two species, there was a significantly lower incidence of male agonism in P. lata. In concordence, analyses of nuclear single-nucleotide polymorphisms showed that P. lata forms large aggregations of unrelated individuals, unlike most Panesthia species, which maintain stable family groups. These results align with previous findings of relaxed intraspecific aggression in island mammals and reptiles, providing novel evidence of behavioural island syndrome in an invertebrate. We also found that courtship behaviour did not vary when P. lata interacted with conspecifics from the same or different populations, suggesting that individuals from different populations will readily interbreed. This is a promising outcome for the conservation of this critically endangered species, which currently spans a fragmentary range consisting of small, insular populations.

evolutionary biology↗

Pleistocene sea-level fluctuation shapes archipelago-wide population structure in the Endangered Lord Howe Island cockroach Panesthia lata

Studies of biogeographic processes have often centred islands as model systems, yet questions remain about the role of Pleistocene sea-level fluctuations in shaping islands biodiversity. One novel, potentially informative model system is the Lord Howe Island Group of Australia. Despite the World Heritage status of this archipelago, almost nothing is known of the biogeographic origins, evolutionary distinctiveness or genetic diversity of the ecological communities across its 28 islands. In this study, we focused on the cockroach Panesthia lata, an ecologically specialized invertebrate with one of the broadest recorded distributions of any LHIG species. To investigate the influence of Pleistocene sea-level fluctuations on LHIG fauna, we explored the phylogeography of P. lata using single-nucleotide polymorphisms and complete mitochondrial genomes. Our analyses reveal that the lineage on the permanently isolated islet Balls Pyramid is highly divergent from the remaining populations, while those on the episodically connected Lord Howe, Roach and Blackburn Islands experienced gene flow during the last glacial period. These results offer the first evidence that Pleistocene land bridges allowed for overland migration across the archipelago. Further, although P. lata was believed to have been locally extirpated by rodents on Lord Howe Island, we discovered two surviving, relict populations. We also detected high levels of inbreeding in all populations, emphasizing the need for ongoing conservation management. Finally, the combination of shallow genetic structure and low diversity suggests that genetic rescue from another island may be a viable strategy to conserve the Lord Howe Island population of P. lata, as well as other species that have been similarly impacted by rodents.

evolutionary biology↗

Decidual natural killer cells promote extravillous trophoblast developmental pathways: evidence from trophoblast organoid co-cultures

The placenta an essential extraembryonic organ that supports the fetus throughout gestation. The interactions between the placenta and the maternal immune system during the first trimester have not been wholly characterized despite their close physical association and hemi-allogeneic relationship. The most abundant type of immune cell in the uterus in the first trimester is the decidual natural killer cell (dNK). Despite their name, dNKs play supportive roles during pregnancy by remodelling uterine spiral arteries. We present evidence suggesting that the matrix metalloproteinases (MMPs) that dNKs secrete to promote this remodelling also drive placental development. This study used a novel co-culture system of dNKs and trophoblast organoids, which are mini-organs representing two to three different cell types of the human placenta. We found that co-cultures for one week led to significant (p=0.020) increases in the organoid area. We also observed significant decreases in trophoblast stemness markers and upregulation of gene sets associated with extravillous trophoblast (EVT) development through bulk RNA sequencing and immunohistochemical examinations. These changes were accompanied by significant (p<0.001) increases in collagen subunit gene expression in the organoids, with simultaneous significant decreases (p<0.001) in the proportion of organoid area occupied by collagen as determined through Massons Trichrome. Cultures containing dNKs also contained significantly higher MMP1, 3, 9, and 10 levels in their culture media, each of which can break down collagen. These findings demonstrate that dNKs promote changes concordant with trophoblast differentiation towards EVTs and villous branching morphogenesis.

developmental biology↗

Plio-Pleistocene decline of mesic forest underpins diversification in a clade of Australian Panesthia cockroaches

The progressive aridification of the Australian continent, and coincident decline of mesic forest, has been a powerful driver of allopatric and environmental speciation in native species. The relictual mesic forests of the eastern seaboard now harbor a diverse group of endemic fauna, including the wood-feeding cockroaches of the genus Panesthia, which reached the continent via two separate invasions from Melanesia. The more recent of these colonization events gave rise to a group of five recognized species, occurring in mainland woodlands, sclerophylls and rainforests, as well as the forests and grasslands of the Lord Howe Island Group. Due to limited sampling in molecular studies and doubt regarding the standing taxonomy, there is little certainty about relationships among the species and poor understanding of the effects of ancient climatic changes upon their evolution. We undertook a comprehensive phylogenetic analysis of the clade, using complete mitogenomes and nuclear ribosomal markers from nearly all known morphospecies and populations. Our time-calibrated phylogenetic analyses reveal six unrecognized, highly divergent lineages, and suggest that these have arisen primarily through vicariance as rainforests fragmented during Plio-Pleistocene glacial cycles (2-5 million years ago). Ancestral niche reconstructions also evidence a tropical rainforest origin for the group, followed by at least three niche transitions into drier forest, including one associated with the singular colonization of the Lord Howe Island Group. Finally, we find evidence of frequent, parallel wing reduction, in potential association with the contraction of forest habitats into small refugia. Our results reiterate the far-reaching role of ancient aridification in driving speciation, niche expansion and morphological evolution in Australian fauna.

evolutionary biology↗

Total-evidence phylogenetic analysis resolves the evolutionary timescale of mantis shrimps (Stomatopoda) and provides insights into their molecular and morphological evolutionary rates

The crustacean order Stomatopoda comprises approximately 500 species of mantis shrimps. These marine predators, common in tropical and subtropical waters, possess sophisticated visual systems and specialized hunting appendages. In this study, we infer the evolutionary relationships within Stomatopoda using a combined data set of 77 morphological characters, whole mitochondrial genomes, and three nuclear markers. Our data set includes representatives from all seven stomatopod superfamilies, including the first sequence data from Erythrosquilloidea. Using a Bayesian relaxed molecular clock with fossil-based calibration priors, we estimate that crown-group unipeltatan stomatopods appeared [~]140 (95% credible interval 201-102) million years ago in the Mesozoic. Additionally, our results support the hypothesis that specialized smashing and spearing appendages appeared early in the evolutionary history of Unipeltata. We found no evidence of a correlation between rates of morphological and molecular evolution across the phylogeny, but identified very high levels of among-lineage rate variation in the morphological characters. Our total-evidence analysis recovered evolutionary signals from both molecular and morphological data sets, demonstrating the merit in combining these sources of information for phylogenetic inference and evolutionary analysis.

evolutionary biology↗

Pervasive relaxed selection in termite genomes

The genetic changes that enabled the evolution of eusociality have long captivated biologists. In recent years, attention has focussed on the consequences of eusociality on genome evolution. Studies have reported higher molecular evolutionary rates in eusocial hymenopteran insects compared with their solitary relatives. To investigate the genomic consequences of eusociality in termites, we sequenced genomes from three of their non-eusocial cockroach relatives. Using a phylogenomic approach, we found that termite genomes experienced lower rates of synonymous mutations than those of cockroaches, possibly as a result of longer generation times. We identified higher rates of nonsynonymous mutations in termite genomes than in cockroach genomes, and identified pervasive relaxed selection in the former (24-31% of the genes analysed) compared with the latter (2-4%). We infer that this is due to a reduction in effective population size, rather than gene-specific effects (e.g., indirect selection of caste-biased genes). We found no obvious signature of increased genetic load in termites, and postulate efficient purging at the colony level. Additionally, we identified genomic adaptations that may underpin caste formation, such as genes involved in post-translational modifications. Our results provide insights into the evolution of termites and the genomic consequences of eusociality more broadly.

evolutionary biology↗

Shrinking in the dark: Parallel endosymbiont genome erosions are associated with repeated host transitions to an underground life

Microbial symbioses have had profound impacts on the evolution of animals. Conversely, changes in host biology may impact the evolutionary trajectory of symbionts themselves. Blattabacterium cuenoti is present in almost all cockroach species and enables hosts to subsist on a nutrient-poor diet. To investigate if host biology has impacted Blattabacterium at the genomic level, we sequenced and analysed 25 genomes from Australian soil-burrowing cockroaches (Blaberidae: Panesthiinae) which have undergone at least seven independent subterranean transitions from above-ground, wood-feeding ancestors. We find at least three independent instances of genome erosion have occurred in Blattabacterium strains exclusive to Australian soil-burrowing cockroaches. Such shrinkages have involved the repeated inactivation of genes involved in amino acid biosynthesis and nitrogen recycling, the core role of Blattabacterium in the host-symbiont relationship. The most drastic of these erosions have occurred in hosts thought to have transitioned underground the earliest relative to other lineages. As Blattabacterium is unable to fulfil its core function in such host groups, our findings suggest soil-burrowing cockroaches must acquire these nutrients from novel sources. Our study represents one of the first cases, to our knowledge, of parallel host adaptations leading to concomitant parallelism in their mutualistic symbionts, further underscoring the intimate relationship between these two partners.

genomics↗

Dating in the Dark: Elevated Substitution Rates in Cave Cockroaches (Blattodea: Nocticolidae) Have Negative Impacts on Molecular Date Estimates

Rates of nucleotide substitution vary substantially across the Tree of Life, with potentially confounding effects on phylogenetic and evolutionary analyses. A large acceleration in mitochondrial substitution rate occurs in the cockroach family Nocticolidae, which predominantly inhabit subterranean environments. To evaluate the impacts of this among-lineage rate heterogeneity on estimates of phylogenetic relationships and evolutionary timescales, we analysed nuclear ultraconserved elements (UCEs) and mitochondrial genomes from nocticolids and other cockroaches. Substitution rates were substantially elevated in nocticolid lineages compared with other cockroaches, especially in mitochondrial protein-coding genes. This disparity in evolutionary rates is likely to have led to different evolutionary relationships being supported by phylogenetic analyses of mitochondrial genomes and UCE loci. Furthermore, Bayesian dating analyses using relaxed-clock models inferred much deeper divergence times compared with a flexible local clock. Our phylogenetic analysis of UCEs, which is the first genome-scale study to include all ten major cockroach families, unites Corydiidae and Nocticolidae and places Anaplectidae as the sister lineage to the rest of Blattoidea. We uncover an extraordinary level of genetic divergence in Nocticolidae, including two highly distinct clades that separated [~]115 million years ago despite both containing representatives of the genus Nocticola. The results of our study highlight the potential impacts of high among-lineage rate variation on estimates of phylogenetic relationships and evolutionary timescales.

evolutionary biology↗

The origin and evolution of mitochondrial tropism in Midichloria bacteria

Midichloria are intracellular bacterial symbionts of ticks. Some representatives of this genus have the unique capability to colonize mitochondria in the cells of their hosts. Hypotheses on the nature of this interaction have proven difficult to test, partly due to a lack of data. Indeed, until now, mitochondrial tropism information and genomes were available only for symbionts of three and two tick host species, respectively. Here we analyzed the mitochondrial tropism of three additional Midichloria and sequenced nine novel genomes, showing that the tropism is pnon-monophyletic, either due to losses of the trait or multiple parallel acquisitions. Comparative genome analyses support the first hypothesis, as the genomes of non-mitochondrial symbionts appear to be reduced subsets of those capable of colonizing the organelles. We detect genomic signatures of mitochondrial tropism, showing a set of candidate genes characteristic of the strains capable of mitochondrial colonization. These include the type IV secretion system and the flagellum, which could allow the secretion of unique effectors, direct interaction with, or invasion of the mitochondria. Other genes, including putative adhesion molecules, proteins possibly involved in actin polymerization, cell wall and outer membrane proteins, are only present in mitochondrial symbionts. The bacteria could use these to manipulate host structures, including mitochondrial membranes, in order to fuse with the organelles or manipulate the mitochondrial network.

evolutionary biology↗

The functional evolution of termite gut microbiota

Termites primarily feed on lignocellulose or soil in association with specific gut microbes. The functioning of the termite gut microbiota is partly understood in a handful of wood-feeding pest species, but remains largely unknown in other taxa. We intend to feel this gap and provide a global understanding of the functional evolution of termite gut microbiota. We sequenced the gut metagenomes of 145 samples representative of the termite diversity. We show that the prokaryotic fraction of the gut microbiota of all termites possesses similar genes for carbohydrate and nitrogen metabolisms, in proportions varying with termite phylogenetic position and diet. The presence of a conserved set of gut prokaryotic genes implies that key nutritional functions were present in the ancestor of modern termites. Furthermore, the abundance of these genes largely correlated with the host phylogeny. Finally, we found that the adaptation to a diet of soil by some termite lineages was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes and pathways. Our results reveal that the composition and function of termite gut prokaryotic communities have been remarkably conserved since termites first appeared [~]150 million years ago. Therefore, the "world smallest bioreactor" has been operating as a multipartite symbiosis composed of termites, archaea, bacteria, and cellulolytic flagellates since its inception.

evolutionary biology↗

Historical biogeography of early diverging termite lineages (Isoptera: Teletisoptera)

Termites are social cockroaches distributed throughout warm temperate and tropical ecosystems. The ancestor of modern termites (crown-Isoptera) occurred during the earliest Cretaceous, approximately 140 million years ago, suggesting that both vicariance through continental drift and overseas dispersal may have shaped the distribution of early diverging termite lineages. We reconstruct the historical biogeography of three early diverging termite families - Stolotermitidae, Hodotermitidae, and Archotermopsidae - using the nuclear rRNA genes and mitochondrial genomes of 27 samples. Our analyses confirmed the monophyly of Stolotermitidae + Hodotermitidae + Archotermopsidae (clade Teletisoptera), with Stolotermitidae diverging from a monophyletic Hodotermitidae + Archotermopsidae approximately 100.3 Ma (94.3-110.4 Ma, 95% HPD), and with Archotermopsidae paraphyletic to a monophyletic Hodotermitidae. The Oriental Archotermopsis and the Nearctic Zootermopsis diverged 50.8 Ma (40.7-61.4 Ma, 95% HPD) before land connections between the Palearctic region and North America ceased to exist. The African Hodotermes + Microhodotermes diverged from Anacanthotermes, a genus found in Africa and Asia, 32.1 Ma (24.8-39.9 Ma, 95% HPD), and the most recent common ancestor of Anacanthotermes lived 10.7 Ma (7.3-14.3 Ma, 95% HPD), suggesting that Anacanthotermes dispersed to Asia using the land bridge connecting Africa and Eurasia [~]18-20 Ma. In contrast, the common ancestors of modern Porotermes and Stolotermes lived 20.2 Ma (15.7-25.1 Ma, 95% HPD) and 26.6 Ma (18.3-35.6 Ma, 95% HPD), respectively, indicating that the presence of these genera in South America, Africa, and Australia involved over-water dispersals. Our results suggest that early diverging termite lineages acquired their current distribution through a combination of over-water dispersals and dispersal via land bridges. We clarify the classification by resolving the paraphyly of Archotermopsidae, restricting the family to Archotermopsis and Zootermopsis, and elevating Hodotermopsinae (Hodotermopsis) as Hodotermopsidae (status novum).

evolutionary biology↗

Evolutionary rates are correlated between Buchnera endosymbionts and mitochondrial genomes of their aphid hosts

The evolution of bacterial endosymbiont genomes is strongly influenced by host-driven selection. Factors affecting host genome evolution will potentially affect endosymbiont genomes in similar ways. One potential outcome is correlations in molecular rates between the genomes of the symbiotic partners. Recently, we presented the first evidence of such a correlation between the mitochondrial genomes of cockroaches and the genome of their endosymbiont (Blattabacterium cuenoti). Here we investigate whether similar patterns are found in additional host-symbiont partners. We use partial genome data from multiple strains of bacterial endosymbionts, B. aphidicola and Sulcia mulleri, and the mitochondrial genomes of their sap-feeding insect hosts. Both endosymbionts show phylogenetic congruence with the mitochondria of their hosts, a result that is expected due to their identical mode of inheritance. We compared root-to-tip distances and branch lengths of phylogenetically independent species pairs. Both analyses show a highly significant correlation of molecular rates between genomes of Buchnera and mitochondrial genomes of their hosts. A similar correlation was detected between Sulcia and their hosts, but was not statistically significant. Our results indicate that evolutionary rate correlations between hosts and long-term symbionts may be a widespread phenomenon.

evolutionary biology↗

SDE2 Integrates into the TIMELESS-TIPIN Complex to Protect Stalled Replication Forks

Protecting replication fork integrity during DNA replication is essential for maintaining genome stability. Here, we report that SDE2, a PCNA-associated protein, plays a key role in maintaining active replication and counteracting replication stress by regulating the replication fork protection complex (FPC). SDE2 directly interacts with the FPC component TIMELESS (TIM) and enhances TIM stability and its localization to replication forks, thereby aiding the coordination of replisome progression. Like TIM deficiency, knockdown of SDE2 leads to impaired fork progression and stalled fork recovery, along with a failure to activate CHK1 phosphorylation. Moreover, loss of SDE2 or TIM results in an excessive MRE11-dependent degradation of reversed forks. Together, our study uncovers an essential role for SDE2 in maintaining genomic integrity by stabilizing the FPC and describes a new role for TIM in protecting stalled replication forks. We propose that TIM-mediated fork protection may represent a way to cooperate with BRCA-dependent fork stabilization.

cell biology↗

Evolutionary rates are correlated between cockroach symbiont and mitochondrial genomes

Bacterial endosymbionts evolve under strong host-driven selection. Factors influencing host evolution might affect symbionts in similar ways, potentially leading to correlations between the molecular evolutionary rates of hosts and symbionts. Although there is evidence of rate correlations between mitochondrial and nuclear genes, similar investigations of hosts and symbionts are lacking. Here we demonstrate a correlation in molecular rates between the genomes of an endosymbiont (Blattabacterium cuenoti) and the mitochondrial genomes of their hosts (cockroaches). We used partial genome data for multiple strains of B. cuenoti to compare phylogenetic relationships and evolutionary rates for 55 cockroach/symbiont pairs. The phylogenies inferred for B. cuenoti and the mitochondrial genomes of their hosts were largely congruent, as expected from their identical maternal and cytoplasmic mode of inheritance. We found a correlation between evolutionary rates of the two genomes, based on comparisons of root-to-tip distances and on comparisons of the branch lengths of phylogenetically independent species pairs. Our results underscore the profound effects that long-term symbiosis can have on the biology of each symbiotic partner.

evolutionary biology↗