Tingru Mao, Yewei Liu, Mariana M. Vasconcellos, Shipeng Zhou, Gajaba Ellepola, Jian Yang, Marcio R. Pie, Madhava Meegaskumbura
{"title":"Caves as species pumps: key innovations, isolation, and periodic introgression drive the world's largest cavefish radiation in a dynamic karstic landscape","authors":"Tingru Mao, Yewei Liu, Mariana M. Vasconcellos, Shipeng Zhou, Gajaba Ellepola, Jian Yang, Marcio R. Pie, Madhava Meegaskumbura","doi":"10.1101/2024.09.12.612638","DOIUrl":"https://doi.org/10.1101/2024.09.12.612638","url":null,"abstract":"Species diversification is shaped by intricate interactions among biotic drivers, including gene flow, hybridization, and key innovations, and abiotic drivers, such as historical climate change, geological events, and ecological opportunity. However, the relative contributions of these drivers in large radiations remain poorly understood. We investigate the interplay among these factors in the diversification of Sinocyclocheilus, a cavefish radiation comprising 79 species. Sinocyclocheilus include typical surface-dwelling forms, with well-developed eyes and pigmentation, to cave-dwelling forms with regressed eyes, reduced pigmentation, and the presence of a horn and a hump. Using reduced representation genomic data (RADseq), we show extensive gene flow events across different species, with introgression playing a key role compared to incomplete lineage sorting in creating phylogenetic discordance and contributing genetic variation for cave adaptation and diversification in this group. Key traits such as eye degeneration, reduced pigmentation, and horn evolved independently multiple times, as adaptations for effectively exploiting cave environments. Furthermore, the uplift of the Tibetan plateau and the late Miocene cooling also significantly impacted speciation rates. Demographic analyses suggest population expansions during the Gonghe Movement and stability during the Last Glacial Maximum, possibly due to cave refugia. Periodic events of introgression promoted by isolation and reconnections due to the changing climate and geological activity, combined with the repeated evolution of key cave-adapted traits, are the primary drivers of this radiation. Our findings underscore the complex interplay of biotic and abiotic factors in the evolution of Sinocyclocheilus fish, offering new insights into the mechanisms of cave adaptation and diversification.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"31 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264673","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Daniel M Wuitchik, James E Fifer, Alexa K Huzar, Jan A Pechenick, Lawrence Uricchio, Sarah W. Davies
{"title":"Outside your shell: how temperature shapes genetic variation in two species of congeneric marine snails","authors":"Daniel M Wuitchik, James E Fifer, Alexa K Huzar, Jan A Pechenick, Lawrence Uricchio, Sarah W. Davies","doi":"10.1101/2024.09.12.612762","DOIUrl":"https://doi.org/10.1101/2024.09.12.612762","url":null,"abstract":"Intertidal organisms withstand extreme temperature fluctuations, and their ability to cope with this variation may affect their distributions across the seascape. Genetic variation and local environments likely interact to determine variation in thermal performance across intertidal species ranges, so characterizing the relationship between temperature variation and population structure is key to understanding the biology of marine invertebrates. Here, we use 2bRAD-sequencing to examine population genetic structure in two congeneric intertidal marine gastropods (Crepidula fornicata, C. plana), sampled from locations along a natural temperature gradient on the Northeast shores of the United States. These two species share similar life histories, yet C. plana exhibits a narrower distribution than C. fornicata. Our results demonstrate that both species show patterns of genetic divergence consistent with isolation by distance, though this pattern was only significant in C. fornicata. Both putatively selected and neutral loci displayed significant spatial structuring in C. fornicata; however, only putatively selected loci showed significant clustering in C. plana. When exploring whether temperature differences explained genetic differentiation, we found that 9-12% of genetic differentiation was explained by temperature variation in each species even when controlling for latitude and neutral population structure. Our results suggest that temperature shapes adaptive variation across the seascape in both Crepidula species and encourages further research to differentiate our results from models of neutral evolutionary drift.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"50 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264670","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Dharani U. Matharage, Riley Cutler, Anamica Khadgi, Amy L. Dapper
{"title":"Inter-strain variation in intra-chromosomal rates of recombination in Caenorhabditis elegans","authors":"Dharani U. Matharage, Riley Cutler, Anamica Khadgi, Amy L. Dapper","doi":"10.1101/2024.09.10.612278","DOIUrl":"https://doi.org/10.1101/2024.09.10.612278","url":null,"abstract":"Meiotic recombination results in the exchange of genetic material between homologous chromosomes. One consequence of meiotic recombination is the production of novel combination of alleles. Recombination rate varies dramatically within and between species, populations, sexes and individuals. Although, the role of PRDM9 in intra-chromosomal variation in crossovers is extensively studied, variation in recombination rate and the cellular and evolutionary dynamics that influence recombination is not well understood due to the complexity of the recombination landscape, intrinsic variation in recombination, and the limited experimental approaches. Though, there has only been limited research regarding the variation in recombination rates in Caenorhabditis elegans, observations from previous studies bring out the potential of C. elegans to be a convenient system for studying intra-chromosomal variation in recombination rate that avoid many of the common pitfalls. Therefore, we investigated the variation in intra-chromosomal patterns of recombination rates in two distinct populations of C. elegans in one of the two high recombination regions of chromosome IV. We used phenotypic fluorescent markers which are inserted in chromosome IV to estimate the recombination rate of the two most genetically distinct strains, N2 and CB4856. We identified statistically significant differences in recombination rate between the two strains, with a 3% higher frequency of recombinant offspring in CB4856 in this focal region. Additionally, we did not find any evidence of sex differences in recombination rate (heterochiasmy). Moreover, we looked at the plasticity of recombination rate in response to stressful conditions in the two C. elegans strains. Here we observed a significant decrease in the recombination rate in both strains when exposed to stressful conditions. These results open the door to using C. elegans to study evolution and genetics of variation in recombination rate.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"22 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205369","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sebastian Jimenez, Naoko P. Kurata, Melanie L. J. Stiassny, S. Elizabeth Alter, Prosanta Chakrabarty, Fernando Alda
{"title":"Complete mitochondrial genomes of riverine Lamprologus (Actinopterygii, Cichlidae) with an emphasis on the blind cichlid L. lethops","authors":"Sebastian Jimenez, Naoko P. Kurata, Melanie L. J. Stiassny, S. Elizabeth Alter, Prosanta Chakrabarty, Fernando Alda","doi":"10.1101/2024.09.11.612419","DOIUrl":"https://doi.org/10.1101/2024.09.11.612419","url":null,"abstract":"Lamprologine cichlids are a diverse group of fishes distributed in Lake Tanganyika and the Congo River. Nine species of Lamprologus occur in the Congo River basin including the only blind cichlid Lamprologus lethops, but little is known about the natural history and evolution of this enigmatic species. To alleviate this knowledge gap, we characterized the complete mitochondrial genomes of L. lethops and its riverine congeners and provided a phylogenetic hypothesis based on these data. We recovered complete mitochondrial genomes from eleven specimens of eight species of Lamprologus. Mitogenomes were identical in the number and order of genes and similar in size (16,579-16,587 bp). In contrast to previous phylogenomic studies, riverine Lamprologus were recovered in two non-sister mitochondrial lineages that were more closely related to other genera of Lake Tanganyika lamprologines than to each other. In the first lineage, most relationships were not highly supported. In the second lineage, L. lethops was recovered as the sister species of L. markerti, L. mocquardi and L. tigripictilis. Interestingly, sequences from L. mocquardi were found in the two mitochondrial lineages. Our results hint at multiple events of past introgression and highlight the importance of increasing taxonomic and genomic sampling to study complex evolutionary histories.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"15 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205371","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nandakishor Krishnan, Ádám Kun, Chaitanya S. Gokhale, József Garay
{"title":"Early eukaryogenesis by host-initiated obligate ectosymbiosis and metabolic inhibition","authors":"Nandakishor Krishnan, Ádám Kun, Chaitanya S. Gokhale, József Garay","doi":"10.1101/2024.09.08.611858","DOIUrl":"https://doi.org/10.1101/2024.09.08.611858","url":null,"abstract":"The evolution of cellular-level symbiosis in microbes is a significant phenomenon to understand the origin of ancestral eukaryotic cells from prokaryotes. Though syntrophy is considered to be the initial interaction mechanism between the involved individuals, the process of internalization (endosymbiosis) and integration to form a symbiotic consortium requires better clarity. This work deals with a theoretical model based on the hypothesis that an intermediate ectosymbiosis might have evolved before complete endosymbiosis. Assuming an already syntrophic environment of free-living hosts and symbionts, we investigate how obligate ectosymbiosis can evolve between the individuals of different species. An asymmetric multilevel selection approach is considered to mechanistically analyze the driving factors in the formation and fixation of the symbiotic consortia. A metabolite-based growth rate and growth inhibition are utilized to effectively model the ecological selection dynamics between the host and the symbiont species. We observed that reduced metabolic growth inhibition due to the effective reduction in exposure to toxic metabolites by the common surface area of contact might be an incentive to stabilize the ectosymbiotic consortia. Furthermore, robust syntrophy between the host and their ectosymbionts might have facilitated obligacy in their association. The model gives insights into the critical elements in the evolution of endosymbiotic features.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"67 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205374","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Lou Guyot, Elizabeth Chahine, Christophe Lalanne, Fanny E Hartmann, Tatiana Giraud
{"title":"Sheltered load in fungal mating-type chromosomes revealed by fitness experiments","authors":"Lou Guyot, Elizabeth Chahine, Christophe Lalanne, Fanny E Hartmann, Tatiana Giraud","doi":"10.1101/2024.09.10.612177","DOIUrl":"https://doi.org/10.1101/2024.09.10.612177","url":null,"abstract":"Sex chromosomes and mating-type chromosomes can carry large regions with suppressed recombination. In these non-recombining regions, recessive deleterious mutations are expected to occur, as i) they are predicted to accumulate as a result of lower efficacy of selection, and ii) they may even pre-exist and drive the evolution of recombination suppression. Multiple genomic analyses have indirectly inferred the presence of deleterious mutations in sex and mating-type chromosomes, but direct experimental evidence remains scarce. Here, we performed fitness assays in fungi with megabase-large and young non-recombining regions around the mating-type locus, using the Schizothecium tetrasporum and Podospora anserina species complexes, to test whether heterokaryons (diploid-like, heterozygous at the mating-type locus) exhibited a fitness advantage over homokaryons (haploid-like, with a single mating-type allele), in terms of spore germination dynamics or mycelium growth speed, under different conditions of light and temperature. We found a faster growth of heterokaryons compared to one of the homokaryons for P. anserina at 18 C, for S. tetrasporum and S. tritetrasporum at 22 C under light, and also at 22 C in the dark for S. tetrasporum. These findings suggest the presence of a sheltered load, i.e. recessive deleterious mutations at the heterozygous state in or near non-recombining regions, as these species are highly homozygous otherwise. Leveraging on the experimental assets of fungi, allowing cultivating separately haploid-like and diploid-like life stages, our experiments provided one of the rare direct experimental evidence of sheltered load around mating-compatibility loci, which is crucial for our understanding of sex-related chromosome evolution.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"67 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205411","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Valeria Anorve-Garibay, Emilia Huerta-Sanchez, Mashaal Sohail, Diego Ortega-Del Vecchyo
{"title":"Natural selection acting on complex traits hampers the predictive accuracy of polygenic scores in ancient samples","authors":"Valeria Anorve-Garibay, Emilia Huerta-Sanchez, Mashaal Sohail, Diego Ortega-Del Vecchyo","doi":"10.1101/2024.09.10.612181","DOIUrl":"https://doi.org/10.1101/2024.09.10.612181","url":null,"abstract":"The prediction of phenotypes from ancient humans has gained interest due to its potential to investigate the evolution of complex traits. These predictions are commonly performed using polygenic scores computed with DNA information from ancient humans along with genome-wide association studies (GWAS) data from present-day humans. However, numerous evolutionary processes could impact the prediction of phenotypes from ancient humans based on polygenic scores. In this work we investigate how natural selection impacts phenotypic predictions on ancient individuals using polygenic scores. We use simulations of an additive trait to analyze how natural selection impacts phenotypic predictions with polygenic scores. We simulate a trait evolving under neutrality, stabilizing selection and directional selection. We find that stabilizing and directional selection have contrasting effects on ancient phenotypic predictions. Stabilizing selection accelerates the loss of large-effect alleles contributing to trait variation. Conversely, directional selection accelerates the loss of small and large-effect alleles that drive individuals farther away from the optimal phenotypic value. These effects result in specific shared genetic variation patterns between ancient and modern populations which hamper the accuracy of polygenic scores to predict phenotypes. Furthermore, we conducted simulations that include realistic strengths of stabilizing selection and heritability estimates to show how natural selection could impact the predictive accuracy of ancient polygenic scores for two widely studied traits: height and body mass index. We emphasize the importance of considering how natural selection can decrease the reliability of ancient polygenic scores to perform phenotypic predictions on an ancient population.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"44 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205414","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Cancer-immune coevolution dictated by antigenic mutation accumulation","authors":"Long Wang, Christo Morison, Weini Huang","doi":"10.1101/2024.09.10.612074","DOIUrl":"https://doi.org/10.1101/2024.09.10.612074","url":null,"abstract":"The immune system is one of the first lines of defence against the emergence of cancer. When effector cells attempt to suppress the tumour, the cancer cells can respond in kind by evolving methods of escape or inhibition. Knowledge of this coevolutionary system and the selection taking place within it can help us understand tumour-immune dynamics both during tumorigenesis but also when treatments such as immunotherapies are applied. Here, we present an individual-based branching process model of mutation accumulation, where random mutations arising in cancer cells trigger corresponding specialised immune responses. Different from previous research, we explicitly model interactions between cancer and effector cells, while incorporating stochastic effects, which are especially important for the expansion and extinction of small populations. We find that the parameters governing interactions between the cancer and effector cells induce different outcomes of tumour progress, such as suppression and evasion. While it is hard to measure the cancer-immune dynamics directly in patients, genetic information of the cancer may indicate the presence of such interactions. Our model demonstrates signatures of selection in sequencing-derived summary statistics, such as the single-cell mutational burden. Thus, bulk and single-cell sequencing of a tumour may give information about the coevolutionary dynamics.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"23 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205410","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Microbiota drives the sexually dimorphic infection outcomes in mealworm beetles","authors":"Srijan Seal, Devashish Kumar, Pavankumar Thunga, Pawan Khangar, Manisha Gupta, Dipendra Nath Basu, Rhitoban Raychoudhury, Imroze Khan","doi":"10.1101/2024.09.10.611485","DOIUrl":"https://doi.org/10.1101/2024.09.10.611485","url":null,"abstract":"Sexually dimorphic responses to pathogenic infections in animals may stem from sex-specific differences in their life history and immune investment. Recent evidence highlights that such sex-specific variations in immune responses can also be critically regulated by microbiota. However, direct experiments to test how microbiota jointly impacts sex-specific immunity and vulnerability to pathogens are still limited. To this end, we used Tenebrio molitor beetles to first establish that sexes appear to differ in their microbiota composition and infection responses. Females were more vulnerable to bacterial infections and carried a higher bacterial load than males. When we depleted the microbiome, only females improved their post-infection survival, leading to a loss of sex-specific infection outcomes. Males, on the other hand, remained unaffected. Microbiota reconstitution (via feeding on faecal matter) of microbiota-depleted females increased their susceptibility to infection again, restoring the sexual dimorphism. We thus found a causal association between microbiome and infection responses. We also found reduced expression of an antimicrobial peptide tenecin 1 in females, which could be associated with their higher infection susceptibility, but such immune gene-vs-phenotypic associations were not consistent across microbiota manipulations. Immune strategies that are required to mediate the causal links between microbiome and infection response might thus vary with microbiota manipulations, warranting future investigations.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"7 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205412","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Epistasis drives rapid divergence across multiple traits during the adaptive evolution of a carbapenemase","authors":"Laura Dabos, Inssaf Nedjari, Alejandro Couce","doi":"10.1101/2024.09.10.610996","DOIUrl":"https://doi.org/10.1101/2024.09.10.610996","url":null,"abstract":"Interactions among beneficial mutations (i.e., epistasis) are often strong enough as to direct adaptation through alternative mutational paths. While alternative solutions should display similar fitness under the primary selective conditions, their properties across secondary environments may differ widely. The extent to which these cryptic differences are to be expected is largely unknown, despite their fundamental and practical importance, such as in the search for exploitable collateral sensitivities among antibiotic resistance mutations. Here we use directed evolution to characterize the diversity of mutational paths through which the prevalent carbapenemase KPC-2 can evolve high activity against the clinically-relevant antibiotic ceftazidime, an initially poor substrate. We identified 40 different substitutions, including many common clinical settings, spread along 18 different mutational trajectories. Initial mutations determined four major groups into which the trajectories can be classified, a signature of strong epistasis. Of note, despite minor variation in final ceftazidime resistance, groups diverged markedly across multiple phenotypic dimensions, from molecular traits such as stability and hydrolitic efficiency to macroscopic traits such as growth rate and activity against other β-lactam antibiotics. Our results indicate that cryptic yet consequential phenotypic differences can readily accumulate under strong selective pressures, bearing implications for efforts to prevent unwanted evolution in microbes.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142205373","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}