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Legendre, F.

Publications and source records attributed to Legendre, F..

7 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↗

Termites became the dominant decomposers of the tropics after two diversification pulses

Insects have the highest species richness among animals, but the extent of their diversity and the timing of their diversification remain unclear. Insect diversification is difficult to infer due to the incompleteness of the fossil record. Phylogenetic trees of extant species reconstructed from an exhaustive sampling can be useful to address major evolutionary questions. Here, we investigated the diversification of termites, which comprise 2,995 described species, using estimates of speciation, extinction, and net diversification rates inferred from molecular phylogenies including 2,800 samples representing 1,377 putative species. Termites originated in the Early Cretaceous [~]132 million years ago. Estimated extinction rates were close to zero despite fossil evidence of extinction; therefore, we focused our interpretations on the net diversification rates. Our analyses detected two significant rate shifts. The first shift occurred at the end of the Cretaceous, initially in the Kalotermitidae, then in the Neoisoptera as they started outcompeting Kalotermitidae. The second shift involved multiple lineages of Neoisoptera, especially Termitidae, which diversified as they colonized the world after the global cooling initiated at the Eocene-Oligocene transition. Our results indicate that termites became the dominant insect decomposers of tropical ecosystems as global climate change impacted ecosystems.

evolutionary biology↗

Cryptocercus genomes expand knowledge of adaptations to xylophagy and termite sociality

Subsociality and wood-eating or xylophagy are understood as key drivers in the evolution of eusociality in Blattodea (cockroaches and termites), two features observed in the cockroach genus Cryptocercus, the sister group of all termites. We present and analyse two new high-quality genomes from this genus, C. punctulatus from North America and C. meridianus from Southeast Asia, to explore the evolutionary transitions to xylophagy and subsociality within Blattodea. Our analyses reveal evidence of relaxed selection in both Cryptocercus and termites, indicating that a reduction in effective population size may have occurred in their subsocial ancestors. These findings challenge the expected positive correlation between dN/dS ratios and social complexity, as Cryptocercus exhibits elevated dN/dS values that may exceed those of eusocial termites. Additionally, we identify positive selection on mitochondrial ribosomal proteins and components of the NADH dehydrogenase complex, suggesting significant evolutionary changes in energy production. Future studies incorporating additional genomic data from diverse blattodean species are essential to elucidate the molecular mechanisms driving transitions to xylophagy and eusociality.

evolutionary biology↗

Reduced regulatory complexity associated with the evolutionary transition to sociality from cockroaches to termites despite evolutionary parallels with Hymenoptera

The degree of phenotypic diversity within social species has previously been associated with more complex genetic regulation both in cis and trans contexts. Transcription factors (TFs) being key to genetic regulation, have been studied in the origins of eusociality in Hymenoptera (bees, ants and wasps) but less so in Blattodea (cockroaches and termites). Here we show that the social transition in Blattodea, from cockroaches to termites, displays similar patterns of regulatory change to those found in Hymenoptera. Specifically, by analysing 3 cockroach and 5 termite genomes, we find more TF families with relaxed selection compared to intensified selection and lineage-specific gene family expansions in termites, which has also been reported in Hymenoptera. We also find that genes under selection support neotenic caste determination. We find there are key differences in Blattodea TF regulation in comparison with Hymenoptera with contractions in TF gene families and no compensatory change in TF DNA binding motifs either in frequency or diversity in TF promoter regions. Furthermore, we show that an increase in social complexity leads to greater diversity in TF activating domains, one of the evolutionary and structural building blocks of TFs, meanwhile, DNA-binding domains, undergo very little change. This study highlights similarities in social transitions between Hymenoptera and Blattodea, with evidence of large changes in transcriptional regulation followed by lineage specific adaptations. Our results indicate that the transcriptional diversity linked to social complexity is not attributable to transcription factors, but is instead likely driven by an alternative mechanism.. Significance statementIt has been widely reported that increased phenotypic complexity, particularly arising from social transitions, is often accompanied by increased regulatory complexity followed by lineage-specific adaptations. While extensively studied in Hymenoptera (bees, ants, and wasps), it has been less explored in Blattodea (cockroaches and termites). By examining the evolution of transcription factors across Blattodea, we investigated the regulatory changes associated with this social transition. Our study reveals that increased social complexity in Blattodea is accompanied by a reduction in regulatory complexity, including decreases in transcription factor numbers and no compensatory change in TF promoter binding site diversity or regulation. This study highlights that social transitions in Blattodea and Hymenoptera share a common pattern of large regulatory changes followed by lineage-specific adaptations.

evolutionary biology↗

The renal inflammatory network of nephronophthisis.

STRUCTURED ABSTRACTO_ST_ABSBACKGROUNDC_ST_ABSThe majority of genetic kidney disease leading to kidney failure is caused by mutations in ciliary genes. How cilia malfunction leads to progressive kidney damage is poorly understood, but recent evidence links ciliopathy genes to CCL2 dependent macrophage recruitment in autosomal dominant polycystic kidney disease (ADPKD), the most studied renal ciliopathy. Whether or not renal inflammation is involved in other renal ciliopathies is unclear. METHODSWe combined mice models with kidney biopsies and renal epithelial cells sampled from human urine to characterize the renal inflammatory network of nephronophthisis (NPH), the most frequent renal ciliopathy in children. RESULTSIn human, mutations in cilia genes involved in NPH enhance urine excretion of the chemokine CCL2, causing abnormal macrophage recruitment in kidney tissues from NPH patients. Differing from ADPKD, inactivating Ccl2 specifically in mouse tubular cells does not rescue the NPH phenotype, suggesting that other inflammatory mediators are involved. Using transcriptional data from 2 NPH models, we identify a set of pro-inflammatory cytokines upregulated in this disease, independently of CCL2. The majority of detectable transcripts from this set are specifically upregulated in kidney cells from NPH patients. In line with the function of these cytokines, NPH kidneys show disproportionate neutrophils and T cells infiltrates compared to healthy subject or hypertensive and diabetic chronic kidney disease patients. CONCLUSIONSThis study reveals that inflammation is a central aspect in human NPH and delineates a specific set of inflammatory mediators that regulates immune cell recruitment in human NPH. SIGNIFICANCE STATEMENTMutations in genes encoding primary cilia proteins are the leading cause of genetic kidney failure. In autosomal dominant polycystic kidney disease (ADPKD), deregulated cilia signaling leads to kidney infiltration by macrophages through the chemokine CCL2. Little is known about renal inflammation in nephronophthisis (NPH), the most frequent pediatric renal ciliopathy. Using NPH mice models, tissues and cells from NPH patients, we unveil renal inflammation as preeminent feature of NPH. Remarkably, the renal inflammatory evoked by ciliary gene mutations in NPH does not overlap with ADPKD: it is CCL2 independent, involves a prominent recruitment of neutrophils and T cells and a specific cytokine signature. This unforeseen findings strengthen the link between primary cilia and renal inflammation.

physiology↗

The Implications of Over-Estimating Gene Tree Discordance on a Rapid-Radiation Species Tree (Blattodea: Blaberidae)

Patterns of discordance between gene trees and the species trees they reside in are crucial to the debate over the superiority of coalescent or concatenation approaches to tree inference. However, errors in estimating gene tree topologies obfuscate the issue by making gene trees appear erroneously discordant with the species tree. We thus test the prevalence of discordance between gene trees and their species tree using an empirical dataset for a clade with a rapid radiation (Blaberidae). We find that one model of codon evolution (FMutSel0) prefers gene trees that are less discordant, while another (SelAC) shows no such preference. We compare the species trees resulting from the selected sets of gene trees on the basis of internal consistency, predictive ability, and congruence with independent data. The species tree resulting from gene trees those chosen by FMutSel0, a set with low discordance, is the most robust and biologically plausible. Thus, we conclude that the results from FMutSel0 are better supported: simple models (i.e., GTR and ECM) infer trees with erroneously high levels of gene tree discordance. Furthermore, the amount of discordance in the set of gene trees has a large effect on the downstream phylogeny. Thus, decreasing gene tree error by lessening erroneous discordance can result in higher quality species trees. These results allow us to support relationships among blaberid cockroaches that were previously in flux as they now demonstrate molecular and morphological congruence.

evolutionary biology↗

Phylogenetic synecdoche demonstrates optimality of subsampling and improves recovery of the Blaberoidea phylogeny

Phylogenomics seeks to use next-generation data to robustly infer an organisms evolutionary history. Yet, the practical caveats of phylogenomics motivates investigation of improved efficiency, particularly when quality of phylogenies are questionable. To achieve improvements, one goal is to maintain or enhance the quality of phylogenetic inference while severely reducing dataset size. We approach this goal by designing an optimized subsample of data with an experimental design whose results are determined on the basis of phylogenetic synecdoche - a comparison of phylogenies inferred from a subsample to phylogenies inferred from the entire dataset. We examine locus mutation rate, saturation, evolutionary divergence, rate heterogeneity, selection, and a priori information content as traits that may determine optimality. Our controlled experimental design is based on 265 loci for 102 blaberoidean cockroaches and 22 outgroup species. High phylogenetic utility is demonstrated by loci with high mutation rate, low saturation, low sequence distance, low rate heterogeneity, and low selection. We found that some phylogenetic information content estimators may not be meaningful for assessing information content a priori. We use these findings to design concatenated datasets with an optimized subsample of 100 loci. The tree inferred from the optimized subsample alignment was largely identical to that inferred from all 265 loci but with less evidence of long branch attraction and improved statistical support. In sum, optimized subsampling can improve tree quality while reducing data collection costs and yielding 4-6x improvements to computation time in tree inference and bootstrapping.

evolutionary biology↗