ORIGINAL ARTICLE
doi:10.1111/evo.13683
Cascading reproductive isolation: Plant phenology drives temporal isolation among populations of a host-specific herbivore
Glen R. Hood,1,2,3 Linyi Zhang,1 Elaine G. Hu,1 James R. Ott,4 and Scott P. Egan1 1Department of Biosciences, Anderson Biological Laboratories, Rice University, Houston, Texas 77005 2Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202 3E-mail: [email protected] 4Population and Conservation Biology Program, Department of Biology, Texas State University, San Marcos, Texas 78666
Received November 5, 2018 Accepted January 7, 2019
All organisms exist within a complex network of interacting species, thus evolutionary change may have reciprocal effects on multiple taxa. Here, we demonstrate “cascading reproductive isolation,” whereby ecological differences that reduce gene flow between populations at one trophic level affect reproductive isolation (RI) among interacting species at the next trophic level. Using a combination of field, laboratory and common-garden studies and long-term herbaria records, we estimate and evaluate the relative contribution of temporal RI to overall prezygotic RI between populations of Belonocnema treatae, a specialist gall- forming wasp adapted to sister species of live oak (Quercus virginiana and Q. geminata). We link strong temporal RI between host-associated insect populations to differences between host plant budbreak phenology. Budbreak initiates flowering and the production of new leaves, which are an ephemeral resource critical to insect reproduction. As flowering time is implicated in RI between plant species, budbreak acts as a “multitrophic multi-effect trait,” whereby differences in budbreak phenology contribute to RI in plants and insects. These sister oak species share a diverse community of host-specific gall-formers and insect natural enemies similarly dependent on ephemeral plant tissues. Thus, our results set the stage for testing for parallelism in a role of plant phenology in driving temporal cascading RI across multiple species and trophic levels.
KEY WORDS: Belonocnema treatae, live oak, multitrophic multieffect trait, Quercus, reproductive isolation.
Ecology plays an essential role in the speciation process when (Talley et al. 2001). However, a synthetic view of how ecologically barriers to gene flow evolve between populations as a result of driven RI arises requires understanding (1) if and how individual ecologically based divergent natural selection (Rundle and Nosil phenotypes are affected by divergent selection between popula- 2005). Thus, knowledge of how such barriers arise is necessary tions experiencing different environments, (2) if those effected for understanding how divergence among populations is initiated phenotypes reduce gene flow between diverging populations, and and maintained. In the last 35 years, the role that ecology plays (3) how multiple barriers accumulate to contribute to RI. during population divergence and the evolution of reproductive To date, a small but growing number of studies have esti- isolation (RI) has been the subject of intensified research (Nosil mated the combined effect of multiple barriers to RI (e.g., Ramsey 2012). Consequently, the study of ecologically based RI has in- et al. 2003; Martin and Willis 2007; Matsubayashi and Katakura creased our understanding of how barriers to gene flow evolve in a 2009; Dopman et al. 2010; Sanchez-Guillen et al. 2012; Lackey diversity of taxa including plants (Richards and Ortiz-Barrientos and Boughman 2017; Paudel et al. 2018; Sambatti et al. 2012). 2016), fishes (Rundle 2002), insects (Feder et al. 1994; Egan However, even for well-studied systems, biologists frequently and Funk 2009), birds (Huber et al. 2007), amphibians (Twomey lack a detailed understanding of the relative contributions of the et al. 2014), reptiles (Rosenblum et al. 2010), and mammals individual components of RI to total RI and/or the chronological