Pollinator-Mediated Isolation May Be an Underestimated Factor in Promoting Homoploid Hybrid Speciation

It is widely acknowledged that allopolyploidy via hybridization and genome doubling can easily lead to speciation, as polyploid hybrids can be immediately isolated from diploid parental taxa due to high levels of sterility caused by uneven numbers of chromosome complements in their progeny (Soltis and Soltis, 2009; Abbott et al., 2013). However, homoploid hybrid speciation (HHS), in which a hybrid lineage becomes genetically isolated from their parents and functions as a distinct evolutionary unit, has been thought to be fairly uncommon (Chase et al., 2010; Servedio et al., 2013). Schumer et al. (2014) proposed three criteria for proving HHS: evidence of hybridization in the genome, reproductive isolation (RI) of hybrid lineages from parental species, and evidence that this reproductive isolation is a consequence of hybridization. According to these criteria, only one case of HHS in sunflowers was strictly documented in plants till now (Schumer et al., 2014). These criteria highlight two reasons why HHS is harder to detect and prove than allopolyploid speciation: the first is the lack of chromosome number change, whereas the second is that molecular evidence for hybridization becomes harder to detect as the parent species become more closely related, and it is known that HHS tends to involve more closely related parent species than allopolyploidy events (Abbott et al., 2013). Inconsistent with the low rate of documented HHS events in plants, a recent simulation study published in PLOS Genetics by Schumer et al. (2015) predicts that homoploid hybrids could rapidly become isolated from parental species by fixing combinations of genes that hinder successful reproduction with parental species, even in the presence of substantial ongoing immigration from parental species to the new homoploid hybrid species. The main reason for the discrepancy might lie in the fact that most population genetics studies are merely focused on evidence of hybridization in the genome, without examining the strength of RI which can be assessed by other integrative methods. Pollination biology approach can address the extent of RI between hybrids and parental species. For example, the detailed examination of flowering time difference and the pattern of pollen flow mediated by pollinator behavior quantified by pollen DNA barcoding method could provide the strength of pre-pollination RI between parental species and hybrids whereas post-pollination RI could be assessed by comparing pollen tube growth and reproductive fitness between parental species and hybrids (e.g., fruit set, seed set, seed viability) using artificial pollination (e.g., Ma …