Toward understanding the genetic mechanisms of speciation: Fine-grained introgressions between species

Abstract The biological species concept (BSC) is the prevailing definition of species whereby genes cannot be exchanged during or after speciation. In contrast, since only genes that contribute to the adaptive divergence between species should be non-exchangeable, BSC appears to bear little relationship to the genetic process of speciation. The rejection of BSC demands evidence of continual gene flow until the completion of speciation. Here, we carry out the sequencing and de novo high-quality assembly of the genomes of two closely related mangrove species (Rhizophora mucronata and R. stylosa). Whole-genome re-sequencing of individuals from their distributions on the tropical coasts shows their genomes to be well delineated in allopatry. They became sympatric in northeastern Australia where their genomes harbor 9,963 and 3,874 introgression blocks, respectively, with each block averaging only about 3-4 Kb. These fine-grained introgressions indicate that gene flow continues even after numerous loci have evolved to become non-introgressable “genomic islets”. Many of these islets, only 1.4 Kb on average, harbor “speciation loci” which contribute to the divergence in flower development or gamete production and thus result in fitness reduction upon introgression. Our fine-grained analysis may thus be the first one to show that gene flow not only happens during speciation, but often continues until the completion of speciation. Under the weight of the extensive literature, BSC may deserve to be retired.

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Genes and the species concept - How much of the genomes can be exchanged?

10.1101/622019 ◽

2019 ◽

Author(s):

Xinfeng Wang ◽

Zixiao Guo ◽

Shaohua Xu ◽

Ming Yang ◽

Qipian Chen ◽

...

Keyword(s):

Species Concept ◽

Biological Species ◽

Biological Species Concept ◽

Full Potential ◽

Mangrove Species ◽

Fine Grained ◽

The Core ◽

Mean Size ◽

Species Specific ◽

The Western Pacific

AbstractIn the biological species concept, much of the genomes cannot be exchanged between species1,2. In the modern genic view, species are distinct as long as genes that delineate the morphological, ecological and reproductive differences remain distinct2. The rest (or the bulk) of the genomes should be freely interchangeable. The core of the species concept therefore demands finding out thefull potentialof introgressions between species. In a survey of two closely related mangrove species (Rhizophora mucronataandR. stylosa) on the coasts of the western Pacific and Indian oceans, we found that the genomes are well delineated in allopatry, echoing their morphological and ecological divergence. The two species are sympatric/parapatric in the Daintree River area of northeastern Australia. In sympatry, their genomes harbor 7,700 and 3,100 introgression blocks, respectively, with each block averaging about 3-4 Kb. These fine-grained and strongly-penetrant introgressions suggest that each species must have evolved many differentially-adaptive (and, hence, non-introgressable) genes that contribute to speciation. We identify 30 such genes, seven of which are about flower development, within small genomic islets with a mean size of 1.4 Kb. In sympatry, the species-specific genomic islets account for only a small fraction (< 15%) of the genomes while the rest appears interchangeable.

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Biological species in the viral world

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1717593115 ◽

2018 ◽

Vol 115 (23) ◽

pp. 6040-6045 ◽

Cited By ~ 20

Author(s):

Louis-Marie Bobay ◽

Howard Ochman

Keyword(s):

Gene Flow ◽

Species Concept ◽

Genome Structure ◽

Biological Species ◽

Arbitrary Sequence ◽

Biological Species Concept ◽

Host Tropism ◽

Universal Definition ◽

Definition Of ◽

Shared Gene

Due to their dependence on cellular organisms for metabolism and replication, viruses are typically named and assigned to species according to their genome structure and the original host that they infect. But because viruses often infect multiple hosts and the numbers of distinct lineages within a host can be vast, their delineation into species is often dictated by arbitrary sequence thresholds, which are highly inconsistent across lineages. Here we apply an approach to determine the boundaries of viral species based on the detection of gene flow within populations, thereby defining viral species according to the biological species concept (BSC). Despite the potential for gene transfer between highly divergent genomes, viruses, like the cellular organisms they infect, assort into reproductively isolated groups and can be organized into biological species. This approach revealed that BSC-defined viral species are often congruent with the taxonomic partitioning based on shared gene contents and host tropism, and that bacteriophages can similarly be classified in biological species. These results open the possibility to use a single, universal definition of species that is applicable across cellular and acellular lifeforms.

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The increasing multiplicity of the species concepts

BSGF - Earth Sciences Bulletin ◽

10.2113/176.2.221 ◽

2005 ◽

Vol 176 (2) ◽

pp. 221-225

Author(s):

Jean Génermont

Keyword(s):

Species Concept ◽

Cladistic Analysis ◽

Biological Species ◽

Point Of View ◽

Biological Species Concept ◽

Phylogenetic Species ◽

Phylogenetic Species Concept ◽

Ecological Criteria ◽

Stem Species ◽

Definition Of

Abstract In 1980, Henri Tintant advocated the usefulness of the biological species concept in paleontology. At this time, this concept was still accepted by many neontologists, but it was already rather severely criticized by some others. In fact, a lot of new concepts appeared in the course of the following two decades. While a few ones are mere adjustments of the biological concept, for instance taking in account ecological criteria, in such a way that it could be applied to clonal organisms, some others, which were developed in connexion with the cladistic theory of taxonomy, are truly new from a conceptual point of view. The diagnosable version of the phylogenetic species concept is somewhat reminiscent of Simpson’s evolutionary species concept, since it accepts phyletic speciation as well as survival of the stem species after a cladogenetic event. One of its more criticizable features, from a cladistic point of view, is that the species are not necessarilly monophyletic. On another hand, according to the monophyly version of the phylogenetic species concept, species are recognized rather subjectively as monophyletic taxa revealed by some previous cladistic analysis dealing with operational taxonomic units. A consensus on the definition of species cannot be expected, since all concepts related to the biological one are founded on population grouping on the basis of potentially identical evolutionary fates, while those which are related to cladistic taxonomy are exclusively concerned with historical features.

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Choke Disease Caused by Epichloë bromicola in the Grass Agropyron repens in Poland

Plant Disease ◽

10.1094/pdis-12-09-0810 ◽

2010 ◽

Vol 94 (11) ◽

pp. 1372-1372 ◽

Cited By ~ 14

Author(s):

M. Lembicz ◽

K. Górzyńska ◽

A. Leuchtmann

Keyword(s):

Sequence Similarity ◽

Original Description ◽

Morphological Characters ◽

Biological Species ◽

Biological Species Concept ◽

Herbarium Specimens ◽

Couch Grass ◽

Definition Of ◽

Choke Disease ◽

Agropyron Repens

Agropyron repens (synonym Elymus repens, couch grass) is a species native to Europe and Asia. In Poland, it is a common weed of crop fields. In May 2008, we noticed for the first time symptoms of choke disease (caused by Epichloë spp.) on A. repens at two localities in central Poland. The localities, Pakość (52°47.531′N, 18°06.118′E) and Dulsk (52°45.329′N, 18°20.518′E), are located 16 km apart from each other. The following year, we confirmed the occurrence of choke disease on couch grass at these localities. Stromata were formed on reproductive stems that did not produce inflorescences. They ranged from 16 to 31 mm long and were covered with perithecia 520 to 560 × 160 to 250 μm at a density of 35 to 45 per mm2. Asci measured 270 to 310 × 5.2 to 6.5 μm and ascospores were 225 to 275 × 1.5 to 1.7 μm (specimen deposited in ZT). Morphological characters match with the original description of Epichloë bromicola (4). One strain was isolated from stromatal tissue and the partial DNA sequence of tubB including introns 1 to 3 was obtained as previously described (2). In a phylogenetic analysis, the isolate (GenBank Accession No. GU325782) grouped with Epichloë isolates from other Agropyron spp. from Poland (A. intermedium) and Japan (A. ciliare and A. tsukushiense) and with an isolate from a Roegneria sp. (from China). Experimental mating tests involving isolates from A. intermedium and a Roegneria sp. indicated that these isolates were sexually compatible with Epichloë bromicola from Bromus erectus. Similarly, E. yangsii was compatible with E. bromicola. This suggests that Epichloë isolates from Agropyron, Roegneria, and Bromus hosts form a common mating population, and implies that under a biological species concept the phylogenetic definition of E. bromicola has to be broadened. Epichloë on A. repens has been previously found in Poland (1), Germany (3), Hungary, and Romania (specimen deposited in herbarium of ETH Zurich, ZT) based on incidental records or on herbarium specimens that have been listed under E. typhina. Our study, based on morphology, tubB sequence similarity, and mating compatibility, suggests that the fungus infecting A. repens in Poland is E. bromicola. References: (1) I. Adamska. Acta Mycol. 36:31, 2001. (2) D. Brem and A. Leuchtmann. Evolution 57:37, 2003. (3) J. Kohlmeyer and E. Kohlmeyer. Mycologia 66:77, 1974. (4) A. Leuchtmann and C. L. Schardl. Mycol. Res. 102:1169, 1998.

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Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1615123114 ◽

2017 ◽

Vol 114 (6) ◽

pp. E1027-E1035 ◽

Cited By ~ 43

Author(s):

Clément Lafon-Placette ◽

Ida M. Johannessen ◽

Karina S. Hornslien ◽

Mohammad F. Ali ◽

Katrine N. Bjerkan ◽

...

Keyword(s):

Gene Flow ◽

Central Europe ◽

Diploid Species ◽

Biological Species ◽

Biological Species Concept ◽

Interspecific Gene Flow ◽

Seed Formation ◽

Arabidopsis Lyrata ◽

Hybrid Seeds ◽

Arabidopsis Arenosa

Based on the biological species concept, two species are considered distinct if reproductive barriers prevent gene flow between them. In Central Europe, the diploid species Arabidopsis lyrata and Arabidopsis arenosa are genetically isolated, thus fitting this concept as “good species.” Nonetheless, interspecific gene flow involving their tetraploid forms has been described. The reasons for this ploidy-dependent reproductive isolation remain unknown. Here, we show that hybridization between diploid A. lyrata and A. arenosa causes mainly inviable seed formation, revealing a strong postzygotic reproductive barrier separating these two species. Although viability of hybrid seeds was impaired in both directions of hybridization, the cause for seed arrest differed. Hybridization of A. lyrata seed parents with A. arenosa pollen donors resulted in failure of endosperm cellularization, whereas the endosperm of reciprocal hybrids cellularized precociously. Endosperm cellularization failure in both hybridization directions is likely causal for the embryo arrest. Importantly, natural tetraploid A. lyrata was able to form viable hybrid seeds with diploid and tetraploid A. arenosa, associated with the reestablishment of normal endosperm cellularization. Conversely, the defects of hybrid seeds between tetraploid A. arenosa and diploid A. lyrata were aggravated. According to these results, we hypothesize that a tetraploidization event in A. lyrata allowed the production of viable hybrid seeds with A. arenosa, enabling gene flow between the two species.

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Genes and speciation: is it time to abandon the biological species concept?

National Science Review ◽

10.1093/nsr/nwz220 ◽

2019 ◽

Vol 7 (8) ◽

pp. 1387-1397 ◽

Cited By ~ 4

Author(s):

Xinfeng Wang ◽

Ziwen He ◽

Suhua Shi ◽

Chung-I Wu

Keyword(s):

Gene Flow ◽

Species Concept ◽

Biological Species ◽

Biological Species Concept ◽

Geographical Isolation ◽

Fundamental Nature ◽

Genomic Analyses ◽

Number Of Genes ◽

The Common ◽

Common Perception

Abstract The biological species concept (BSC) is the cornerstone of neo-Darwinian thinking. In BSC, species do not exchange genes either during or after speciation. However, as gene flow during speciation is increasingly being reported in a substantial literature, it seems time to reassess the revered, but often doubted, BSC. Contrary to the common perception, BSC should expect substantial gene flow at the onset of speciation, not least because geographical isolation develops gradually. Although BSC does not stipulate how speciation begins, it does require a sustained period of isolation for speciation to complete its course. Evidence against BSC must demonstrate that the observed gene flow does not merely occur at the onset of speciation but continues until its completion. Importantly, recent genomic analyses cannot reject this more realistic version of BSC, although future analyses may still prove it wrong. The ultimate acceptance or rejection of BSC is not merely about a historical debate; rather, it is about the fundamental nature of species – are species (and, hence, divergent adaptations) driven by a relatively small number of genes, or by thousands of them? Many levels of biology, ranging from taxonomy to biodiversity, depend on this resolution.

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An overview of speciation and species limits in birds

The Auk ◽

10.1093/ornithology/ukab006 ◽

2021 ◽

Author(s):

Kevin Winker

Keyword(s):

Gene Flow ◽

Integrative Taxonomy ◽

Difficult Problem ◽

Biological Species ◽

Biological Species Concept ◽

Species Limits ◽

Main Driver ◽

Data Signal ◽

Clear Line ◽

Silver Bullet

Abstract Accurately determining avian species limits has been a challenge and a work in progress for most of a century. It is a fascinating but difficult problem. Under the biological species concept, only lineages that remain essentially independent when they are in sympatry are clearly species. Otherwise, there is no clear line yet found that marks when a pair of diverging lineages (e.g., in allopatry) become different enough to warrant full biological species status. Also, with more data, species limits often require reevaluation. The process of divergence and speciation is itself very complex and is the focus of intense research. Translating what we understand of that process into taxonomic names can be challenging. A series of issues are important. Single-locus criteria are unlikely to be convincing. Genetic independence is not a species limits requirement, but the degree of independence (gene flow) needs to be considered when there is opportunity for gene flow and independence is not complete. Time-based species (limits determined by time of separation) are unsatisfactory, though integrating time more effectively into our datasets is warranted. We need to disentangle data signal due to neutral processes vs. selection and prioritize the latter as the main driver of speciation. Assortative mating is also not likely to be an adequate criterion for determining species limits. Hybridization and gene flow are more important than ever, and there is a condition not being treated evenly in taxonomy: evolutionary trysts of 2 or more lineages stuck together through gene flow just short of speciation over long periods. Comparative methods that use what occurs between good species in contact to infer species limits among allopatric forms remain the gold standard, but they can be inaccurate and controversial. Species-level taxonomy in birds is likely to remain unsettled for some time. While the study of avian speciation has never been more exciting and dynamic, there is no silver bullet for species delimitation, nor is it likely that there will ever be one. Careful work using integrative taxonomy in a comparative framework is the most promising way forward.

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Fine-grained adaptive divergence in an amphibian: genetic basis of phenotypic divergence and the role of nonrandom gene flow in restricting effective migration among wetlands

Molecular Ecology ◽

10.1111/mec.12181 ◽

2013 ◽

Vol 22 (5) ◽

pp. 1322-1340 ◽

Cited By ~ 35

Author(s):

Alex Richter-Boix ◽

María Quintela ◽

Marcin Kierczak ◽

Marc Franch ◽

Anssi Laurila

Keyword(s):

Gene Flow ◽

Genetic Basis ◽

Adaptive Divergence ◽

Fine Grained ◽

Phenotypic Divergence

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Birds of Prey (Falconiformes, Accipitriformes) of Northern Eurasia in the Biological Tetranary Nomenclature

Raptors Conservation ◽

10.19074/1814-8654-2020-40-16-51 ◽

2020 ◽

pp. 16-51

Author(s):

Pavel V. Pfander ◽

◽

Keyword(s):

Reproductive Isolation ◽

Species Concept ◽

Physical Object ◽

Biological Species ◽

Birds Of Prey ◽

Northern Eurasia ◽

Biological Species Concept ◽

Species Problem ◽

Nomenclature System ◽

Definition Of

The main disadvantage of the generally accepted trinary system of around-species nomenclature is the lack of a species concept. This leads to the fact that any lower taxon can be declared a species or subspecies, and any combination of these taxa of arbitrary rank is correct and legitimate, by definition, and therefore cannot even be discussed. Ambiguity of the level of divergence of species creates a “species problem” and makes the question – species or subspecies – meaningless. The solution to the “species problem” can be the creation of a nomenclature system with a "own" species concept. The only concept whose criteria are objective (reproductive isolation and sympatry) and, more importantly, correspond to a certain level of divergence, and that have a biological meaning, is a biological species concept. However, the use of this concept is difficult due to the uncertainty of the degree of reproductive isolation. Therefore, a revised definition of a biological species (B-species) as a category of taxonomy is proposed – this is a level of divergence that provides reproductive isolation sufficient for sympatry (with other closely related forms). Accordingly, as a physical object, the B-species can be defined as a set of sister populations that are incapable to sympatry with each other. The level of B-species is very high, therefore, for forms intermediate between subspecies and B-species, an additional category is needed – a semi-species. Unlike subspecies, which differ only in size and color, a semi-species must have at least one of the following features: 1 – obvious differences in the preference for environmental conditions; 2 – a certain assortative mating with other semi-species; 3 – reduced fertility of hybrids; 4 – significant differences in morphology, physiology, behavior, etc.; 5 – the hybridization zone is relatively very narrow (parapatry). The taxonomy of birds of prey (Falconiformes, Accipitriformes) of Northern Eurasia is presented in a new (genus, B-species, semi-species, subspecies) system of categories and nomenclature.

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Sympatric and allopatric differentiation delineates population structure in free-living terrestrial bacteria

10.1101/644468 ◽

2019 ◽

Author(s):

Alexander B. Chase ◽

Philip Arevalo ◽

Eoin L. Brodie ◽

Martin F. Polz ◽

Ulas Karaoz ◽

...

Keyword(s):

Gene Flow ◽

Isolation By Distance ◽

Biological Species ◽

Microbial Populations ◽

Marker Genes ◽

Rrna Gene ◽

Biological Species Concept ◽

Free Living ◽

Species Definition ◽

Isolation By Environment

ABSTRACTIn free-living bacteria and archaea, the equivalent of the biological species concept does not exist, creating several barriers to the study of the processes contributing to microbial diversification. As such, microorganisms are often operationally defined using conserved marker genes (i.e., 16S rRNA gene) or whole-genome measurements (i.e., ANI) to interpret intra-specific processes. However, as in eukaryotes, investigations into microbial populations must consider the potential for interacting genotypes among individuals that are subjected to similar environmental selective pressures. Therefore, we isolated 26 strains within a single bacterial ecotype (equivalent to a eukaryotic species definition) from a common habitat (leaf litter) across a regional climate gradient and asked whether the genetic diversity in a free-living soil bacterium (Curtobacterium) was consistent with patterns of allopatric or sympatric differentiation. By examining patterns of gene flow, our results indicate that microbial populations are delineated by gene flow discontinuities and exhibit evidence for population-specific adaptation. We conclude that the genetic structure within this bacterium is due to both adaptation within localized microenvironments (isolation-by-environment) as well as dispersal limitation between geographic locations (isolation-by-distance).

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