Hybridization without guilt: gene flow and the biological species concept

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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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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Discriminating arboviral species

Journal of General Virology ◽

10.1099/jgv.0.001572 ◽

2021 ◽

Vol 102 (4) ◽

Author(s):

Yiyuan Li ◽

Angela C. O’Donnell ◽

Howard Ochman

Keyword(s):

Evolutionary History ◽

Viral Vectors ◽

Species Concept ◽

International Committee ◽

Biological Species ◽

Biological Species Concept ◽

Substantial Variation ◽

Artificial Boundaries ◽

Human Infections

Mosquito-borne arboviruses, including a diverse array of alphaviruses and flaviviruses, lead to hundreds of millions of human infections each year. Current methods for species-level classification of arboviruses adhere to guidelines prescribed by the International Committee on Taxonomy of Viruses (ICTV), and generally apply a polyphasic approach that might include information about viral vectors, hosts, geographical distribution, antigenicity, levels of DNA similarity, disease association and/or ecological characteristics. However, there is substantial variation in the criteria used to define viral species, which can lead to the establishment of artificial boundaries between species and inconsistencies when inferring their relatedness, variation and evolutionary history. In this study, we apply a single, uniform principle – that underlying the Biological Species Concept (BSC) – to define biological species of arboviruses based on recombination between genomes. Given that few recombination events have been documented in arboviruses, we investigate the incidence of recombination within and among major arboviral groups using an approach based on the ratio of homoplastic sites (recombinant alleles) to non-homoplastic sites (vertically transmitted alleles). This approach supports many ICTV-designations but also recognizes several cases in which a named species comprises multiple biological species. These findings demonstrate that this metric may be applied to all lifeforms, including viruses, and lead to more consistent and accurate delineation of viral species.

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Putting the Biological Species Concept to the Test: Using Mating Networks to Delimit Species

PLoS ONE ◽

10.1371/journal.pone.0068267 ◽

2013 ◽

Vol 8 (6) ◽

pp. e68267 ◽

Cited By ~ 5

Author(s):

Lélia Lagache ◽

Jean-Benoist Leger ◽

Jean-Jacques Daudin ◽

Rémy J. Petit ◽

Corinne Vacher

Keyword(s):

Species Concept ◽

Biological Species ◽

Biological Species Concept

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Fern nothogenera and ×Lepinema, a new hybrid genus between Ellipinema and Lepisorus (Polypodiaceae)

Phytotaxa ◽

10.11646/phytotaxa.455.4.3 ◽

2020 ◽

Vol 455 (4) ◽

pp. 262-266

Author(s):

LIANG ZHANG ◽

LI-BING ZHANG

Keyword(s):

Species Concept ◽

Intergeneric Hybrid ◽

Molecular Data ◽

Biological Species ◽

Biological Species Concept

The biological species concept is not exclusively applicable in many groups of organisms including ferns. Interspecific fern hybrids are not rare: there are 16 intergeneric hybrid genera in ferns confirmed with molecular data. Here we add one more hybrid genus in the tribe Lepisoreae of Polypodiaceae, ×Lepinema, formed via hybridization between parents in two genera: Ellipinema and Lepisorus.

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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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Charles Darwin's biological species concept and theory of geographic speciation: the transmutation notebooks

Annals of Science ◽

10.1080/00033797800200251 ◽

1978 ◽

Vol 35 (3) ◽

pp. 275-297 ◽

Cited By ~ 34

Author(s):

Malcolm J. Kottler

Keyword(s):

Species Concept ◽

Biological Species ◽

Biological Species Concept

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Group selection and the development of the biological species concept

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2010.0040 ◽

2010 ◽

Vol 365 (1547) ◽

pp. 1853-1863 ◽

Cited By ~ 8

Author(s):

James Mallet

Keyword(s):

Species Concept ◽

Biological Species ◽

Second World War ◽

Species Level ◽

Biological Species Concept ◽

Ernst Mayr ◽

World War ◽

Mutualistic Interaction ◽

Theodosius Dobzhansky ◽

Second World

The development of what became known as the biological species concept began with a paper by Theodosius Dobzhansky in 1935, and was amplified by a mutualistic interaction between Dobzhansky, Alfred Emerson and Ernst Mayr after the second world war. By the 1950s and early 1960s, these authors had developed an influential concept of species as coadapted genetic complexes at equilibrium. At this time many features of species were seen as group advantages maintained by selection to avoid breakdown of beneficial coadaptation and the ‘gene pool’. Speciation thus seemed difficult. It seemed to require, more so than today, an external deus ex machina , such as allopatry or the founder effect, rather than ordinary within-species processes of natural selection, sexual selection, drift and gene flow. In the mid-1960s, the distinctions between group and individual selection were clarified. Dobzhansky and Mayr both understood the implications, but their views on species changed little. These group selectionist ideas now seem peculiar, and are becoming distinctly less popular today. Few vestiges of group selectionism and species-level adaptationism remain in recent reviews of speciation. One wonders how many of our own cherished views on evolution will seem as odd to future biologists.

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Collembola, the biological species concept and the underestimation of global species richness

Molecular Ecology ◽

10.1111/mec.12472 ◽

2013 ◽

Vol 22 (21) ◽

pp. 5382-5396 ◽

Cited By ~ 38

Author(s):

Francesco Cicconardi ◽

Pietro P. Fanciulli ◽

Brent C. Emerson

Keyword(s):

Species Richness ◽

Species Concept ◽

Biological Species ◽

Biological Species Concept

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Predictors of Taxonomic Inflation and its Role in Primate Conservation

10.1101/2021.09.10.459781 ◽

2021 ◽

Author(s):

Maria J.A. Creighton ◽

Alice Q. Luo ◽

Simon M. Reader ◽

Arne Ø. Mooers

Keyword(s):

Perceived Risk ◽

Species Concept ◽

Research Effort ◽

Biological Species ◽

Primate Species ◽

Biological Species Concept ◽

Primate Conservation ◽

Phylogenetic Species Concept ◽

Initial Application ◽

Positive Message

ABSTRACTSpecies are the main unit used to measure biodiversity, but different preferred diagnostic criteria can lead to very different delineations. For instance, named primate species have more than doubled since 1982. Such increases have been termed “taxonomic inflation” and have been attributed to the widespread adoption of the ‘phylogenetic species concept’ (PSC) in preference to the previously popular ‘biological species concept’ (BSC). Criticisms of the PSC have suggested taxonomic inflation may be biased toward particular taxa and have unfavourable consequences for conservation. Here, we explore predictors of taxonomic inflation across primate taxa since the initial application of the PSC nearly 40 years ago. We do not find evidence that diversification rate, the rate of lineage formation over evolutionary time, is linked to inflation, contrary to expectations if the PSC identifies incipient species. We also do not find evidence of research effort in fields where work has been suggested to motivate splitting being associated with increases in species numbers among genera. To test the suggestion that splitting groups is likely to increase their perceived risk of extinction, we test whether genera that have undergone more splitting have also observed a greater increase in their proportion of threatened species since the introduction of the PSC. We find no cohesive signal of inflation leading to higher threat probabilities across primate genera. Overall, this analysis sends a positive message that threat statuses of primate species are not being overwhelmingly affected by splitting in line with what has recently been reported for birds. Regardless, we echo warnings that it is unwise for conservation to be reliant on taxonomic stability. Species (however defined) are not independent from one another, thus, monitoring and managing them as such may not meet the overarching goal of conserving biodiversity.

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