Alistair Vance
University of Manchester
Abstract
The question “What is a species?” remains one of the most fundamental and contentious issues in biology. This review synthesizes the historical evolution of species concepts, focusing on the theoretical and practical conflicts between the Biological Species Concept (BSC) and the Phylogenetic Species Concept (PSC). We examine how the advent of large-scale genomics and metagenomics has profoundly challenged these traditional frameworks, particularly when applied to microbes and asexually reproducing organisms. Phenomena such as horizontal gene transfer (HGT) and extensive cryptic diversity have revealed the limitations of concepts based on reproductive isolation or simple phylogenetic branching. In response, the scientific community has developed new genomic-based frameworks, such as those using Average Nucleotide Identity (ANI) thresholds, which offer operational consistency but raise new questions about the nature of species boundaries. This review explores the ongoing philosophical debate between species concept pluralism and the search for a unified concept, demonstrating how this tension manifests in practical fields like conservation biology, where the choice of concept directly impacts legal protection and resource allocation. We conclude by analyzing the unresolved questions and future directions, emphasizing the growing consensus around integrative, multicriteria approaches that reconcile the complexity of evolutionary processes with the need for a stable and practical taxonomic system.
Keywords:
1. Introduction: The Enduring Species Problem
Species delimitation is a central challenge in evolutionary biology, with profound implications for taxonomy, ecology, conservation, and our fundamental understanding of biodiversity. The frameworks used to define species have been shaped by a century of intense theoretical debate and major paradigm shifts (Wheeler & Meier, 2000; Zachos, 2018). The 20th century was
dominated by the Biological Species Concept (BSC), which was formalized by Ernst Mayr and defines species as “groups of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups” (Wheeler & Meier, 2000). This emphasis on reproductive isolation provided a clear, process-based criterion that became foundational to the Modern Synthesis.
However, the late 20th and early 21st centuries witnessed a paradigm shift driven by advances in molecular systematics and phylogenetics. Dissatisfaction with the BSC’s inapplicability to asexual organisms, fossils, and hybridizing taxa led to the rise of lineage-based concepts, most notably the Phylogenetic Species Concept (PSC). The PSC defines a species as “the smallest diagnosable cluster of individual organisms within which there is a parental pattern of ancestry and descent,” shifting the focus from interbreeding to diagnosable, monophyletic lineages (Wheeler & Meier, 2000; Padial & De la Riva, 2020). Other concepts, like the Ecological Species Concept (ESC), further enriched the debate by defining species as groups of organisms adapted to a particular ecological niche (Sites & Marshall, 2004).
This conceptual evolution has been radically accelerated by the “meta-data era” of genomics and metagenomics (Jiao et al., 2024). High-throughput sequencing has exposed the limitations of all traditional concepts, especially in the microbial world, which is characterized by asexual reproduction, rampant horizontal gene transfer (HGT), and vast unculturable diversity (Konstantinidis, 2023). This review will synthesize the literature to trace this complex journey. We will first outline the foundational assumptions and historical conflicts between the major species concepts. Second, we will analyze how the genomic revolution has systematically challenged these frameworks, with a special focus on the microbial world. Third, we will explore the high-level philosophical debate between species concept pluralism and unification, and finally, we will examine the tangible, real-world consequences of these debates for fields like conservation biology, concluding with a look at the unresolved questions that will define the future of taxonomy.
2. The Conceptual Foundation: A History of Competing Ideas
The conflict between the BSC and PSC is rooted in their different foundational assumptions. The BSC assumes that reproductive isolation is the necessary and sufficient criterion for species status, a powerful mechanism for maintaining species cohesion in sexually reproducing organisms. In contrast, the PSC assumes that diagnosability based on unique character states—whether morphological or genetic—is sufficient to delimit a species, regardless of reproductive potential (Wheeler & Meier, 2000; Zachos, 2018). The ESC adds another dimension, postulating that species are defined by the ecological niche they occupy, thus linking taxonomy directly to function (Sites & Marshall, 2004).
These differing assumptions lead to profoundly different practical outcomes. The BSC is most applicable to sexually reproducing organisms but is largely irrelevant for asexuals and fossils.
The PSC and ESC, however, are universally applicable in theory, as all organisms have an evolutionary history and an ecological context (Wheeler & Meier, 2000). This leads to a well-documented “lumper vs. splitter” dynamic: the BSC’s focus on interbreeding potential tends to “lump” populations into fewer, larger species, whereas the PSC’s focus on fine-scale diagnosable differences often leads to “splitting” taxa into a greater number of smaller species (Zachos, 2018). Consequently, the BSC promotes greater taxonomic stability, while the PSC can lead to more frequent and dynamic taxonomic revisions as new data emerge (Twyford et al., 2024).
Empirical studies confirm that these concepts are not interchangeable. In a study of 15 frog species, only four (27%) showed full congruence when assessed with morphological, reproductive, and phylogenetic evidence, highlighting the need for integrative taxonomy (Padial et al., 2009). The choice of concept is therefore not a matter of preference but a decision with significant scientific consequences.
3. The Genomic Revolution and the Microbial Challenge
The advent of large-scale genomic and metagenomic sequencing has acted as a stress test for all traditional species concepts, revealing their shortcomings with unprecedented clarity, particularly in the microbial world.
3.1. How Genomics Undermines Traditional Concepts
Genomic data have exposed four key limitations of traditional species definitions when applied to microbes. First, they have shown that cultivation-based methods are profoundly biased, missing the vast majority of microbial diversity, now often termed “dark taxa” (Rodriguez-R & Konstantinidis, 2014; Wijayawardene et al., 2021). Second, phenotype-genotype discordance is rampant; microbes with similar appearances can be genetically divergent, while genetically similar microbes can exhibit high phenotypic plasticity (Rodriguez-R & Konstantinidis, 2014). Third, genomics has confirmed that horizontal gene transfer (HGT) is a dominant force in prokaryotic evolution. The frequent exchange of genes across deep phylogenetic divides blurs the very notion of a vertically inherited, tree-like history of descent, which is a core assumption of the PSC (Hall et al., 2020; Syvanen, 2012).
Fourth, and perhaps most importantly, genomics reveals that microbial diversity is often organized into sequence-discrete clusters, but with blurry, not sharp, boundaries. While large-scale studies consistently find a statistical gap in Average Nucleotide Identity (ANI) at around 95% between bacterial clusters, which is often used as a de facto species threshold, intermediate forms are also common (Konstantinidis, 2023; Olm et al., 2020). This evidence supports the existence of species-like units but simultaneously challenges any rigid, universal definition.
3.2. The Emergence of Genomic-Based Frameworks
In response to these challenges, a new suite of genomic-based frameworks has emerged. The 95% ANI threshold has become a widely used operational criterion for delimiting prokaryotic species, as it aligns with natural breaks in homologous recombination efficiency, which drops sharply below this level of identity (Bobay & Ochman, 2017; Konstantinidis, 2023). This provides a modern, gene-flow-based reinterpretation of the BSC that is applicable to microbes.
To manage the explosion of genomic data, resources like the Genome Taxonomy Database (GTDB) have been developed. GTDB provides a standardized, phylogenetically consistent classification for both cultured and uncultured taxa based on genome-wide ANI and relative evolutionary divergence (Chuvochina et al., 2023). In parallel, nomenclatural systems like SeqCode propose using genome sequences as formal “type material” for naming uncultured organisms, solving a long-standing procedural bottleneck in taxonomy (Chuvochina et al., 2023).
These genomic tools have proven to be of immense practical value. In microbial ecology, they reveal functional differences between generalist and specialist taxa that correlate with genome size and gene content (Loos et al., 2022). In clinical microbiology, metagenomic next-generation sequencing (mNGS) vastly outperforms culture-based methods for pathogen identification, demonstrating a diagnostic accuracy of 74.9% compared to 36.9% for conventional tests (Wu et al., 2022).
4. High-Level Debates and Real-World Consequences
The turmoil at the practical level of species delimitation reflects a deeper, long-standing philosophical debate in biology: should we embrace a pluralism of species concepts, or strive for a single, unified theory?
4.1. Species Concept Pluralism vs. Unification
The existence of over 22 documented species concepts is a testament to species concept pluralism, an approach that provides operational flexibility by allowing researchers to choose the concept best suited to their study organism and question (R., 2009). However, this flexibility comes at the cost of ambiguity and a lack of standardization, which hinders comparability across studies. For example, different bioinformatic pipelines using different underlying assumptions and reference databases yield divergent results for species identification from the same dataset (Hiergeist et al., 2023).
In response, philosophers of science like Kevin de Queiroz have championed a unified species concept, arguing that all species can be universally defined as “segments of separately evolving lineages” (Queiroz, 2005). In this hierarchical framework, properties like reproductive isolation, diagnosability, or ecological niche are not defining criteria themselves but rather secondary lines of evidence (or “operational criteria”) used to identify those lineages. This approach provides theoretical clarity while still allowing for methodological flexibility. The genomic data revealing sequence-discrete clusters in microbes (Konstantinidis, 2023) lends strong support to this lineage-based view, but the prevalence of HGT continues to challenge any simplistic interpretation of what constitutes a “separate” lineage (Hall et al., 2020).
4.2. A Case Study in Consequences: Conservation Biology
Nowhere are the practical consequences of this debate more apparent than in conservation biology. The choice between the BSC (a “lumper”) and the PSC (a “splitter”) has significant legal, policy, and management implications. A quantitative survey found that applying the PSC increases the number of recognized species by an average of 48% compared to non-phylogenetic concepts (Agapow et al., 2004).
This “taxonomic inflation” means that each newly recognized species has, by definition, a smaller population size and a more restricted geographic range, making it more likely to qualify for protection under legal frameworks like the IUCN Red List or the U.S. Endangered Species Act (Zachos, 2018; Betts et al., 2020). While this approach can be praised for highlighting and protecting cryptic diversity that the BSC would overlook, it creates immense practical challenges. It can dilute finite conservation funding across a larger number of units and lead to “taxonomic instability,” where frequent revisions to species lists undermine long-term management planning and legal enforcement (Martin et al., 2022). The BSC, while offering more stability, risks under-protecting significant evolutionary diversity by lumping distinct lineages into a single managed unit (Zachos, 2018).
5. Discussion and Future Directions
The journey from Mayr’s BSC to the GTDB reflects a profound evolution in how we conceptualize life’s diversity. It is now clear that no single, simple species concept is sufficient. The BSC fails in the face of asexual reproduction and HGT; the PSC can be confounded by gene flow and arbitrary marker choices; and the ESC is often difficult to operationalize due to a lack of ecological data, especially for microbes (Sites & Marshall, 2004; Hahn et al., 2021).
The central unresolved question is how to reconcile the messy reality of pervasive gene flow—via both hybridization and HGT—with the practical need for a stable and coherent taxonomic system. The current consensus is coalescing around integrative, multicriteria
approaches. These frameworks, which align with the unified species concept’s philosophy, use a primary evolutionary lineage concept as a theoretical foundation but rely on multiple, independent lines of evidence—genomic, ecological, morphological, and reproductive—to delimit species robustly (Fišer et al., 2018; Padial et al., 2009).
Significant challenges remain. First, there is a pressing need to standardize methodologies and nomenclatural systems, especially for the vast “dark taxa” of uncultured microbes (Chuvochina et al., 2023). Second, computational methods must continue to improve to accurately model both vertical descent and horizontal gene flow simultaneously (Jackson et al., 2016; Sánchez-Soto et al., 2020). Finally, the scientific community must remain transparent about the conceptual assumptions underlying any taxonomic decision to ensure reproducibility and facilitate progress.
6. Conclusion
The species problem is not a problem to be solved but rather a complex and dynamic field of inquiry that evolves with our understanding of the natural world. Historically, the debate was dominated by the conflict between the process-based BSC and the pattern-based PSC. The genomic revolution has shattered the simplicity of this dichotomy, revealing a world of cryptic diversity, porous species boundaries, and rampant horizontal gene transfer that challenges all traditional frameworks.
In the face of this complexity, the most promising path forward lies in a pragmatic synthesis: a unified, lineage-based theoretical concept operationalized through a flexible, integrative, and multicriteria approach. By combining the power of whole-genome data with ecological, phenotypic, and reproductive evidence, we can build a taxonomic system that is both evolutionarily realistic and practically useful. The definition of a species may never be simple, but by embracing this complexity, we move closer to a classification that truly reflects the intricate and interconnected tapestry of life.
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