Introduction
Speciation is often defined as a process in which one species splits
into two. However, new species can also form as a result of
hybridization between different species (Abbott, 1992; Rieseberg, 1997;
Mallet, 2007; Soltis & Soltis, 2010). This occurs most commonly when
hybridization is accompanied by whole genome duplication (i.e.,
allopolyploid speciation). The genome duplication provides partial
reproductive isolation between the new allopolyploid lineage and its
parental species, which eases establishment (Baack et al., 2015). Less
commonly, a new hybrid lineage establishes and becomes reproductively
independent without a change in ploidy level (i.e., homoploid hybrid
speciation). The ecological and evolutionary conditions necessary for
homoploid hybrid speciation are more restrictive than for allopolyploidy
because of the lack of a universal mechanism for creating reproductive
isolation between the hybrid lineages and its parental species (Buerkle
et al., 2000, 2003; Schumer et al., 2015; Comeault, 2018; Blanckaert et
al., 2018, 2023).
Allopolyploidy is also easier to document than homoploid hybrid
speciation because hybridization and whole genome duplication are
readily detected from cytological and genomic data. Thus, the prevalence
of allopolyploidy is fairly well established (Wood et al., 2009; Mayrose
et al., 2011; Barker et al., 2016). In contrast, the frequency of
homoploid hybrid speciation remains unclear, mainly because
hybridization can lead to outcomes other than speciation, including
maladaptive, neutral, or adaptive introgression, genetic swamping,
outbreeding depression, stable hybrid zones, reinforcement, etc., and it
can be difficult to distinguish between these different outcomes (Abbott
et al., 2013; Taylor & Larson, 2019; Bock et al., 2023). Also, these
outcomes are not mutually exclusive. For example, while some
introgressions may be maladaptive and contribute to outbreeding
depression, others from the same donor species could enhance local
adaption and/or reproductive isolation (Schumer et al., 2018).
In an attempt to reduce this uncertainty, Schumer et al. (2014) put
forward three criteria for establishing homoploid hybrid speciation: (1)
reproductive isolation from the parental species; (2) evidence of
previous admixture; and (3) demonstration that reproductive barriers are
derived via hybridization. While criteria one and two are relatively
straightforward to demonstrate, showing that hybridization led to the
formation of reproductive isolation is more challenging. Indeed, Schumer
et al. (2014) argued that only one butterfly species (Maverez et al.
2006) and three sunflower species (Rieseberg et al., 2003, but see Owens
et al., 2023) satisfied all three criteria. Others have worried that the
criteria may be too stringent and that a focus on reproductive isolation
might shift attention away from other important aspects of the process
such as ecological divergence and the generation of evolutionary novelty
(Nieto Feliner et al., 2017; Wang, Xu et al., 2022). Also, in some
instances biological mechanisms of reproductive isolation may not be
critical to homoploid hybrid speciation, such as in the Oxford ragwort
(Senecio Squalidus ), where the homoploid hybrid is allopatric
with its parental species (James & Abbott, 2005; Nieto Feliner et al.,
2017). These concerns have led to the suggestion that homoploid hybrid
species be classified as type 1 when reproductive isolation is a direct
result of hybridization and type 2 when reproductive isolation is a
by-product of other processes (Ottenburghs, 2018).
An important consequence of this debate has been an increased focus on
the potential role of hybridization in the evolution of reproductive
isolation between hybrid lineages and their parental species (Schumer et
al., 2018; Ottenburghs, 2018; Brennan et al., 2019). Partly as a result,
there now are more than a dozen cases of homoploid hybrid speciation in
which the evolution of reproductive barriers has been directly linked to
hybridization (Salazar et al., 2010; Hermansen et al., 2014; Lukhtanov
et al., 2015; Leducq et al., 2016; Lamichhaney et al., 2018; Brennan et
al., 2019; Masello et al., 2019; Sun et al., 2020; Wang et al., 2021;
Stevison et al., 2022; Wang, Kang et al., 2022; Zou et al., 2022; Wu et
al., 2023; Zhang et al., 2023). More importantly, genomics approaches
have been developed that offer a straightforward means for showing that
the reproductive barriers isolating new homoploid hybrid species from
their parents are indeed derived from hybridization (Sun et al., 2020;
Wang et al., 2021). In this comment, we discuss a particularly effective
strategy for making such connections that was developed by Jianquan Liu
and his colleagues (Figure 1), the application of this method to several
plant and animal species, and what we have learned about homoploid
hybrid speciation as a consequence (Wang et al., 2021; Wang, Kang et
al., 2022; Zou et al., 2022; Wu et al., 2023; Zhang et al., 2023).