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The Howard & Moore Complete Checklist of the Birds of theWorld: framework for species delimitation
Manuel Schweizer, David A. Marques, Urban Olsson &Pierre‐André Crochet
COPYRIGHT: © 2023 Schweizer, Marques, Olsson & Crochet. This is an article distributed under
the terms of the Creative Commons Attribution Licence, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original authors and source arecredited.
KEYWORDS: avian systematics, birds, speciation, species criteria, species delimitation, species
concept, reproductive isolation.
INTRODUCTION

The core of any taxonomic checklist comprises species‐level delimitations. These should
be made as consistent as possible among different taxa, within a single checklist but also
between checklists and major taxonomic groups, and thus follow a common framework. Thisconcise text explains the guidelines for species delimitation applied in the process of gradually
updating the Howard & Moore Complete Checklist of the Birds of the World (4th Edition) as it
evolves into an online list with continuous updating. This text is not aimed at providing acomprehensive review on different species concepts and species delimitation procedures, butinstead explains the basis used in the Howard & Moore Checklist for assessing species rank ofvalid taxa. It is not an entirely new or original approach, as it draws its foundations fromprevious publications on speciation, species concepts or guidelines for taxonomic decisions
and has previously been employed in other groups of animals (e.g., Speybroeck et al., 2020).
BACKGROUND

Most biologists would probably agree that variation in nature is generally not continuous;
however, there may be no single optimal way to divide this discontinuity into different species(cf. Sangster, 2018). Species can generally be considered as separately evolving
metapopulation lineages or distinct branches in a phylogenetic tree (De Queiroz, 2007).
However, while it is clear that all species are distinct evolutionary lineages, it does not followthat all such lineages can be considered to be species (cf. Hillis, 2019, 2020). This is because
speciation, the evolution of reproductive isolation between distinct evolutionary lineages
allowing them to ultimately coexist in the same location (Mayr, 1942), is a continuous process.
Speciation can be considered as achieved with the attainment of complete reproductive
isolation between two evolutionary lineages (e.g., Coyne & Orr, 2004), although it has to beacknowledged that it is neither a deterministic, nor necessarily is speciation an irreversible
process before complete reproductive incompatibility is achieved. Moreover, speciation does
not need to be completed for lineages to be ranked as species, because diverging lineages may
attain enough reproductive isolation to maintain distinct gene pools without complete
geographical isolation while still possessing the ability to produce viable hybrid offspring or
hybrid populations.
Any framework or guiding principles for species delimitation should be approached bymaking the distinction between the species concept, i.e., a theoretical framework describing

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what species are, and the species criteria used to delimit species in practice (Mayden, 1997; cf.
Sangster, 2018).
SPECIES CONCEPT AND SPECIES DELIMITATION CRITERIAThe Howard & Moore Complete Checklist of the Birds of the World (5th Edition) aims torecognize as species those lineages that have acquired substantial reproductive isolation inaccordance with the biological species concept (Mayr, 1942). Reproductive isolation is thus
considered as the most important criterion for species delimitation as it is the prerequisite for
evolutionary lineages to maintain their integrity through space and time (cf. Helbig et al., 2002).
The first major difficulty with that criterion is that reproductive isolation is measurable only
when lineages are in direct contact, e.g., in sympatry or parapatry. As speciation in birds
usually proceeds through an initial phase in allopatry (Phillimore et al., 2008; Price, 2008),
many closely related, but geographically separated lineages cannot directly be assessed forspecies status using the reproductive isolation criterion. The second major difficulty with thecriterion of reproductive isolation is that, even though hybridization is generally rare on an
individual level (Mayr, 2014; Justyn et al., 2020), mating between different species has been
documented for a large number of widely recognized bird species often accompanied by geneflow across species boundaries (Grant & Grant, 1992; Mallet, 2005; McCarthy, 2006; Price, 2008;
Rheindt & Edwards, 2011). This indicates that even though strong reproductive isolation canevolve in birds on short time scales of 1–2 million years or much less (Weir & Price, 2011), its
completion can take much longer (Price & Bouvier, 2002) and postzygotic compatibility may
remain in place for a long time between lineages that are isolated by prezygotic mechanisms.
Proponents of the biological species concept have argued that some level of hybridization andgene flow between evolutionary lineages should not preclude their treatment as species‐leveltaxa, unless it leads to a complete merging of their gene pools and consequently the loss of
their distinctness (Coyne & Orr, 2004). Consequently, for the Howard & Moore Checklist,
speciation does not need to have reached complete reproductive isolation for lineages to be
ranked as species. Instead, we regard as species distinct evolutionary lineages that exhibit
enough reproductive isolation to coexist durably in sympatry or parapatry or that have
evolved a degree of distinctness in allopatry that would make coexistence in sympatry orparapatry likely. Taxa connected through populations of admixed origin (such as hybrid
zones) are treated as valid species if barriers against interspecific gene flow exist and are strong
enough to ensure persistence of their distinct gene pools over evolutionary time scales (e.g.,maintenance of a narrow hybrid zone).
CRITERIA FOR RANKING TAXA AS SPECIESThe Howard & Moore Checklist applies the following species criteria to assess the statusof evolutionary lineages under the biological species concept by focusing on reproductive
isolation as defining the criteria.
In the simplest case, evolutionary lineages coexist in sympatry and show complete
reproductive isolation, i.e., reproduction occurs only within a group and not among groups
and are thus considered different species. Besides direct observation of reproductive
behaviour, e.g., of mate choice or offspring parental identity, proxies such as genetic,
morphological, vocal, behavioural, and ecological differentiation may be used to indirectly
assess reproductive isolation among such sympatric lineages. In more difficult cases, where(i) reproductive isolation cannot be assessed directly, i.e., in allopatric lineages, or (ii) where

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reproductive isolation is incomplete, i.e., hybridizing lineages in sympatry or parapatry, thestatus is assessed as follows:i) In the case of allopatric lineages, multiple lines of evidence are taken into account toassess the potential for the existence of reproductive isolation in a hypothetical scenario when
the two lineages in question would meet in parapatry or sympatry. As a proxy for the potential
existence of reproductive isolation, we evaluate their degree of divergence compared toclosely related taxa that are demonstrated to be valid species. Data on the genotype and thephenotype, such as physiology, morphology, vocalization, behaviour as well as ecology are
considered in an integrative way — taking into account all available evidence without
requiring evidence to be available for every type of data (Sangster, 2018). Species rank is
assigned when evolutionary lineages with strict allopatric distributions differ using various
proxies at similar levels to those exhibited by closely related pairs of taxa that are
reproductively isolated and unambiguously assigned to species rank, as proposed by Helbig
et al., (2002). However, as reproductive isolation can evolve largely independently of
divergence in phenotype, ecology or genotype (Stankowski & Ravinet, 2021) and intrinsic
postzygotic barriers can evolve in morphologically cryptic lineages that additionally doneither differ obviously in sexual signalling nor in ecology (Pulido‐Santacruz et al., 2018;
Cronemberger et al., 2020), we do not apply any form of scoring of character differences
between evolutionary lineages for establishing species limits based on predefined thresholds(Tobias et al., 2010; Donegan, 2018). Such a scoring approach may overlook substantial cryptic
diversity given the relative and highly variable nature of the speciation process acrosslineages, and moreover, despite what is advocated by its proponents, it often suffers from low
reproducibility (Rheindt & Ng, 2021). Instead, we assess multiple lines of available evidence
taking into account time of divergence as well as lineage‐specific characters that vary between
well‐established species of the same lineage and/or are involved in reproductive isolation inthat specific lineage.
ii) In the case of evolutionary lineages distributed in parapatry or sympatry that do notshow complete reproductive isolation, we apply the following criteria to identify species rank.
For sympatric lineages, the circumstances of gene flow should suggest they will not lead tothe complete merging of their gene pools and the loss of their distinctness (Coyne & Orr, 2004).
Lineages that exhibit a parapatric distribution with a hybrid zone as the result of secondary
contact are considered species when sufficient barriers to gene flow away from the hybridzone prevent the complete merging of the two distinct gene pools by taking into account that
selection against introgression often varies across the genome and parts might be merged.
Such barriers to introgression may include assortative mating, i.e., preferential mating within
species, or reduced fitness of hybrids or admixed genotypes compared to parental lineages in
the hybrid zone or in their respective ranges. Examples of potential proxies of such barriers
include estimates of gene flow across hybrid zones from multilocus genetic data based on
many independently evolving genetic markers, or especially from neutral alleles (Westram etal., 2022); linkage disequilibrium of multiple unlinked genetic regions differentiated between
lineages (Poelstra et al., 2014; Toews et al., 2016); bi‐ or multimodal trait or genotype
distributions in hybrid zones (Gay et al., 2008); or patterns of mate choice in contact zones(Brambilla et al., 2008). Such proxies are considered again in an integrative way, considering
all available evidence without requiring evidence to be available for each proxy (Sangster,2018), to evaluate whether gene pools of parapatric lineages are likely to remain distinct.
Species should generally be monophyletic, unless there is evidence for rapid (peripatric)or hybrid speciation (Hermansen et al., 2011; Elgvin et al., 2017) or the prevalence of‘combinatorial mechanisms’ — the reassembly of old genetic variants into novel combinations

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Avian Systematics 2023 1 (IX): N35–N41(Marques et al., 2019) — during the speciation process that could leave some taxa to become
paraphyletic. As a consequence, we also use phylogenetic relationships (branching patterns inaddition to divergence) to assess species limits whenever information on reproductive
isolation is missing (unstudied contact zones or allopatric lineages). However, phylogenetic
hypotheses should preferably not be evaluated on the basis of single non‐recombining units
such as mtDNA (so‐called gene trees), as phylogenetic reconstruction based on or dominatedby such types of data (i.e., mtDNA combined with a few uninformative nuclear data) do notnecessarily represent the true history of lineages (the so‐called species tree). Stochastic
processes resulting in incomplete lineage sorting, introgression (e.g., Edwards, 2009; Edwards& Bensch, 2009; Toews & Brelsford, 2012) including retention of haplotypes resulting fromancient introgression of an extinct species (Hogner et al., 2012; Zhang et al., 2019), or non‐neutral evolution (Pavlova et al., 2013; Fossoy et al., 2016), can generate discordance between
gene trees and the species tree. We thus caution against drawing taxonomic conclusions solely
based on phylogenetic hypotheses stemming from mtDNA. Nonetheless, phylogenetic
analyses and estimates on divergence times from single‐marker studies are important
supporting information for delimitation of lineages supported by multiple lines of evidence,and these can be compared to those between other closely related lineages unambiguously
assigned to species rank.
CONCLUDING REMARK

By applying a biological species concept and focusing on the defining criteria ofreproduction isolation as the cornerstone of the speciation process, we apply a prospective
approach (cf. Sangster, 2018). Species delimitation decisions are thus made on the basis ofpresent‐day or potential future processes or interactions among lineages. To evaluate whether
lineages are likely to fuse in the future, our approach relies on integrating multiple lines ofevidence by evaluating all present data. Consequently, species delimitation decisions concern
hypotheses that need to be documented and reevaluated when new evidence becomes
available.
One common criticism to the use of the biological species concept as a basis for speciesdelimitation is the subjectivity involved on where to cut the speciation continuum for ranking
taxa connected by hybrid zones and for ranking allopatric taxa. We fully acknowledge thisdifficulty but wish to point out that the use of other delimitation criteria under alternative
species concepts come with the same level of subjectivity. For example, defining species as“separately evolving metapopulation lineages” under a unified species concept (de Queiroz,
2007) requires in our opinion a similar amount of subjectivity to assess how much “separation”
is enough to grant species rank. However, the use of the the isolation version of the biological
species concept presents the advantage of having a clear definition of what speciation is: theevolution of reproductive isolation.
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Addresses
Manuel Schweizer (), Naturhistorisches Museum, Bern, Switzerland and Institute of Ecology and
Evolution, University of Bern, Bern, Switzerland.
e‐mail: manuel.schweizer@nmbe.ch.
David A. Marques, Naturhistorisches Museum Basel, Switzerland.
e‐mail: David.Marques@bs.ch.
Urban Olsson, Department of Biological and Environmental Sciences, University of Gothenburg, P.O.
Box 463, SE‐405 30 Gothenburg, Sweden and Gothenburg Global Biodiversity Centre, P.O. Box 461,
SE‐405 30 Gothenburg, Sweden.
e‐mail: urban.olsson@bioenv.qu.se.
Pierre‐André Crochet, CEFE, CNRS, Univ. Montpellier, EPHE, IRD, Montpellier, France.
e‐mail: pierre‐andre.crochet@cefe.cnrs.fr.

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