The role of hybrid seed inviability in angiosperm speciation

Abstract

Understanding which reproductive barriers contribute to speciation is essential to understanding the diversity of life on earth. Several contemporary examples of strong hybrid seed inviability (HSI) between recently diverged species suggest that HSI may play a fundamental role in plant speciation. Yet, a broader synthesis of HSI is needed to clarify its role in diversification. Here, I review the incidence and evolution of HSI. Hybrid seed inviability is common and evolves rapidly, suggesting that it may play an important role early in speciation. The developmental mechanisms that underlie HSI involve similar developmental trajectories in endosperm, even between evolutionarily deeply diverged incidents of HSI. In hybrid endosperm, HSI is often accompanied by whole‐scale gene misexpression, including misexpression of imprinted genes which have a key role in endosperm development. I explore how an evolutionary perspective can clarify the repeated and rapid evolution of HSI. In particular, I evaluate the evidence for conflict between maternal and paternal interests in resource allocation to offspring (i.e., parental conflict). I highlight that parental conflict theory generates explicit predictions regarding the expected hybrid phenotypes and genes responsible for HSI. While much phenotypic evidence supports a role of parental conflict in the evolution of HSI, an understanding of the underlying molecular mechanisms of this barrier is essential to test parental conflict theory. Lastly, I explore what factors may influence the strength of parental conflict in natural plant populations as an explanation for why rates of HSI may differ between plant groups and the consequences of strong HSI in secondary contact.

Limited reproductive interference despite high rates of heterospecific pollen transfer among co‐occurring bat‐pollinated Burmeistera

“…Post‐pollination reproductive barriers can occur at various stages between pollen deposition and ovule fertilization. Early‐acting barriers operate in the stigma or the distal part of the style arresting pollen germination and early pollen‐tube growth, whereas late‐acting barriers occur farther toward the base of the style and the entrance to ovules, preventing fertilization, or during the postzygotic phase, causing abnormal embryo development, hybrid seed abortion, or inviability (Ashman and Arceo‐Gómez, 2013; Moreira‐Hernández and Muchhala, 2019; Coughlan, 2023). Thus, early‐acting barriers are more effective at limiting reproductive interference because as heterospecific pollen germinates and the tube grows down the style, the opportunities for negatively affecting conspecific pollen success increase (Ashman and Arceo‐Gómez, 2013).…”

The role of conflict in shaping plant biodiversity

“…Hybridization between populations with different historical levels of conflict can cause a mismatch in paternally derived resource‐acquiring and maternally derived resource‐repressive alleles, resulting in parent‐of‐origin specific growth abnormalities and inviability (Haig & Westoby, 1991; Zeh & Zeh, 2000). In angiosperms, the endosperm nourishes offspring, is itself a product of fertilization, and is overwhelmingly the site of imprinted expression (Coughlan, 2023a). Parental conflict therefore predicts that: the endosperm should exhibit parent‐of‐origin growth abnormalities; and imprinted genes that regulate nutrient partitioning from mothers to developing offspring should underlie hybrid seed inviability (Coughlan, 2023a).…”

“…Hybrid seed inviability is common and rapidly evolving in angiosperms (Fig. 1; Coughlan, 2023a). Much evidence supports the assertion that hybrid seed inviability is prevalent among species with different mating systems or other demographic factors that are predicted to influence the strength of parental conflict (Brandvain & Haig, 2005; Städler et al ., 2021).…”

“…Akin to the idea that repeated evolution of phenotypes in similar environments is strong evidence of natural selection (Endler, 1986), the extent of parallelism of intrinsic postzygotic incompatibilities may also serve as evidence that particular types of natural selection are responsible for their evolution. For example, the observation that hybrid seed inviability typically involves repeated over‐ or undergrowth endosperm phenotypes, even in organisms with different endosperm developmental programs that are diverged > 150 Ma, provides strong evidence that hybrid seed inviability as a class of incompatibilities may evolve via parental conflict (Coughlan, 2023a). Similarly, CMS consistently involves the loss of pollen (Rieseberg & Blackman, 2010).…”

“…Pointed arrow denotes a transcription factor that increases expression, while a blunted arrow denotes a transcription factor that reduces expression. This panel is based on Coughlan (2023a). Roth and Florez‐rueda (2019) proposes an alternative model in which divergence at genes which control dosage‐sensitive processes causes widespread misexpression and inviability (model not shown).…”