Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: Simulations and empirical data from pine‐feeding hymenopterans

Abstract

Although haplodiploidy is widespread in nature, the evolutionary consequences of this mode of reproduction are not well characterized. Here, we examine how genome‐wide hemizygosity and a lack of recombination in haploid males affects genomic differentiation in populations that diverge via natural selection while experiencing gene flow. First, we simulated diploid and haplodiploid “genomes” (500‐kb loci) evolving under an isolation‐with‐migration model with mutation, drift, selection, migration and recombination; and examined differentiation at neutral sites both tightly and loosely linked to a divergently selected site. As long as there is divergent selection and migration, sex‐limited hemizygosity and recombination cause elevated differentiation (i.e., produce a “faster‐haplodiploid effect”) in haplodiploid populations relative to otherwise equivalent diploid populations, for both recessive and codominant mutations. Second, we used genome‐wide single nucleotide polymorphism data to model divergence history and describe patterns of genomic differentiation between sympatric populations of Neodiprion lecontei and N. pinetum, a pair of pine sawfly species (order: Hymenoptera; family: Diprionidae) that are specialized on different pine hosts. These analyses support a history of continuous gene exchange throughout divergence and reveal a pattern of heterogeneous genomic differentiation that is consistent with divergent selection on many unlinked loci. Third, using simulations of haplodiploid and diploid populations evolving according to the estimated divergence history of N. lecontei and N. pinetum, we found that divergent selection would lead to higher differentiation in haplodiploids. Based on these results, we hypothesize that haplodiploids undergo divergence‐with‐gene‐flow and sympatric speciation more readily than diploids.

Whole Genomes Reveal Evolutionary Relationships and Mechanisms Underlying Gene-Tree Discordance inNeodiprionSawflies

“…4). More generally, interspecific gene flow has been pervasive in the Lecontei group (Linnen and Farrell 2007; Bendall et al 2022; Fig. 4), a scenario for which SVDquartets may outperform ASTRAL and other locus-based approaches (Long and Kubatko 2018; Wascher and Kubatko 2021).…”

“…Specifically, we focus on the eastern North American “ Lecontei ” clade of Neodiprion sawflies (Order: Hymenoptera, Family: Diprionidae). Previous studies suggest that this clade radiated with substantial gene flow sometime within the last 2-10 million years (Linnen and Farrell 2007, 2008b; Bendall et al 2022). Upon colonizing eastern North America, population divergence and speciation were likely driven by rapid adaptation to new Pinus hosts (Linnen and Farrell 2010; Bagley et al 2017; Bendall et al 2017; Glover et al 2023).…”

Body size as a magic trait in two plant-feeding insect species

“…First, a recent demographic analysis supports a sympatric divergence scenario for N. lecontei and N. pinetum (Bendall et al 2022). Second, N. lecontei and N. pinetum are not completely reproductively isolated: viable and fertile hybrids can be produced in the lab (Bendall et al 2017, 2021) and these species are known to hybridize in some parts of their ranges (Bendall et al 2022). Incomplete isolation is essential for distinguishing between reproductive barriers that cause speciation versus those that accrue only after it is complete (Coyne and Orr 2004; Nosil 2012).…”

Asymmetric Inheritance: The Diversity and Evolution of Non-Mendelian Reproductive Strategies

“…Female-producing parthenogenesis (thelytoky) occurs in different formsit can be obligate, sperm-dependent, facultative, spontaneous or cyclical (reviewed in Jalvingh et al 2016). Obligate parthenogenetic animal species are rare compared to sexual species, but widespread across most major taxa (Bell 1982). The vast majority of the taxonomically described parthenogenetic species represent independent transitions to parthenogenesis as most of these species are "tips on the tree of life", meaning there are few genera or higher taxa consisting solely of parthenogenetic species (Bell 1982).…”