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      Sperm‐dependent asexual species and their role in ecology and evolution

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          Abstract

          Sexual reproduction is the primary mode of reproduction in eukaryotes, but some organisms have evolved deviations from classical sex and switched to asexuality. These asexual lineages have sometimes been viewed as evolutionary dead ends, but recent research has revealed their importance in many areas of general biology. Our review explores the understudied, yet important mechanisms by which sperm‐dependent asexuals that produce non‐recombined gametes but rely on their fertilization, can have a significant impact on the evolution of coexisting sexual species and ecosystems. These impacts are concentrated around three major fields. Firstly, sperm‐dependent asexuals can potentially impact the gene pool of coexisting sexual species by either restricting their population sizes or by providing bridges for interspecific gene flow whose type and consequences substantially differ from gene flow mechanisms expected under sexual reproduction. Secondly, they may impact on sexuals' diversification rates either directly, by serving as stepping‐stones in speciation, or indirectly, by promoting the formation of pre‐ and postzygotic reproduction barriers among nascent species. Thirdly, they can potentially impact on spatial distribution of species, via direct or indirect (apparent) types of competition and Allee effects. For each such mechanism, we provide empirical examples of how natural sperm‐dependent asexuals impact the evolution of their sexual counterparts. In particular, we highlight that these broad effects may last beyond the tenure of the individual asexual lineages causing them, which challenges the traditional perception that asexual lineages are short‐lived evolutionary dead ends and minor sideshows. Our review also proposes new research directions to incorporate the aforementioned impacts of sperm‐dependent asexuals. These research directions will ultimately enhance our understanding of the evolution of genomes and biological interactions in general.

          Abstract

          Asexual species play important roles in the ecology and evolution of ecosystems. Our review highlights the many ways asexuals can influence sexual species.

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          Most cited references172

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          The landscape of Neandertal ancestry in present-day humans

          Analyses of Neandertal genomes have revealed that Neandertals have contributed genetic variants to modern humans 1–2 . The antiquity of Neandertal gene flow into modern humans means that regions that derive from Neandertals in any one human today are usually less than a hundred kilobases in size. However, Neandertal haplotypes are also distinctive enough that several studies have been able to detect Neandertal ancestry at specific loci 1,3–8 . Here, we have systematically inferred Neandertal haplotypes in the genomes of 1,004 present-day humans 12 . Regions that harbor a high frequency of Neandertal alleles in modern humans are enriched for genes affecting keratin filaments suggesting that Neandertal alleles may have helped modern humans adapt to non-African environments. Neandertal alleles also continue to shape human biology, as we identify multiple Neandertal-derived alleles that confer risk for disease. We also identify regions of millions of base pairs that are nearly devoid of Neandertal ancestry and enriched in genes, implying selection to remove genetic material derived from Neandertals. Neandertal ancestry is significantly reduced in genes specifically expressed in testis, and there is an approximately 5-fold reduction of Neandertal ancestry on chromosome X, which is known to harbor a disproportionate fraction of male hybrid sterility genes 20–22 . These results suggest that part of the reduction in Neandertal ancestry near genes is due to Neandertal alleles that reduced fertility in males when moved to a modern human genetic background.
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            Horizontal gene transfer in prokaryotes: quantification and classification.

            Comparative analysis of bacterial, archaeal, and eukaryotic genomes indicates that a significant fraction of the genes in the prokaryotic genomes have been subject to horizontal transfer. In some cases, the amount and source of horizontal gene transfer can be linked to an organism's lifestyle. For example, bacterial hyperthermophiles seem to have exchanged genes with archaea to a greater extent than other bacteria, whereas transfer of certain classes of eukaryotic genes is most common in parasitic and symbiotic bacteria. Horizontal transfer events can be classified into distinct categories of acquisition of new genes, acquisition of paralogs of existing genes, and xenologous gene displacement whereby a gene is displaced by a horizontally transferred ortholog from another lineage (xenolog). Each of these types of horizontal gene transfer is common among prokaryotes, but their relative contributions differ in different lineages. The fixation and long-term persistence of horizontally transferred genes suggests that they confer a selective advantage on the recipient organism. In most cases, the nature of this advantage remains unclear, but detailed examination of several cases of acquisition of eukaryotic genes by bacteria seems to reveal the evolutionary forces involved. Examples include isoleucyl-tRNA synthetases whose acquisition from eukaryotes by several bacteria is linked to antibiotic resistance, ATP/ADP translocases acquired by intracellular parasitic bacteria, Chlamydia and Rickettsia, apparently from plants, and proteases that may be implicated in chlamydial pathogenesis.
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              A new evolutionary law

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                Author and article information

                Contributors
                janko@iapg.cas.cz
                schlupp@ou.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                28 September 2023
                October 2023
                : 13
                : 10 ( doiID: 10.1002/ece3.v13.10 )
                : e10522
                Affiliations
                [ 1 ] Laboratory of Non‐Mendelian Evolution, Institute of Animal Physiology and Genetics Academy of Sciences of the Czech Republic Liběchov Czech Republic
                [ 2 ] Department of Biology and Ecology, Faculty of Science University of Ostrava Ostrava Czech Republic
                [ 3 ] Department of Zoology, Faculty of Natural Sciences Comenius University in Bratislava Bratislava Slovakia
                [ 4 ] Department of Plant Developmental Genetics, Institute of Biophysics Academy of Sciences of the Czech Republic Brno Czech Republic
                [ 5 ] Department of Biology University of Oklahoma Oklahoma Norman USA
                [ 6 ] Department of Biology International Stock Center for Livebearing Fishes Oklahoma Norman USA
                Author notes
                [*] [* ] Correspondence

                Karel Janko, Laboratory of Non‐Mendelian Evolution, Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, Liběchov, Czech Republic.

                Email: janko@ 123456iapg.cas.cz

                Ingo Schlupp, Department of Biology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA.

                Email: schlupp@ 123456ou.edu

                Author information
                https://orcid.org/0000-0002-2460-5667
                Article
                ECE310522 ECE-2023-04-00610.R1
                10.1002/ece3.10522
                10534198
                37780083
                500916c9-7fa4-4d77-8b75-8d18a180b403
                © 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 August 2023
                : 11 January 2023
                : 24 August 2023
                Page count
                Figures: 10, Tables: 0, Pages: 21, Words: 16599
                Funding
                Funded by: Grantová Agentura České Republiky , doi 10.13039/501100001824;
                Award ID: 21‐25185S
                Funded by: National Science Foundation, Division of Environmental Biology
                Award ID: 1916519
                Funded by: Ministerstvo školstva, vedy, výskumu a športu Slovenskej republiky , doi 10.13039/501100003193;
                Award ID: APVV‐19‐0076
                Funded by: Institutional Research Concept RVO
                Award ID: 67985904
                Funded by: Ministry of Education, Youth and Sports of the Czech Republic
                Award ID: 539 EXCELLENCE CZ.02.1.01/0.0/0.0/1 5_003/0000460 OP RDE
                Categories
                Evolutionary Ecology
                Review Article
                Review Articles
                Custom metadata
                2.0
                October 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.4 mode:remove_FC converted:28.09.2023

                Evolutionary Biology
                apparent competition,hybridization,meiosis,population dynamics,speciation
                Evolutionary Biology
                apparent competition, hybridization, meiosis, population dynamics, speciation

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