Evolutionary genetics of host shifts in herbivorous insects: insights from the age of genomics

Abstract

Adaptation to different host taxa is a key driver of insect diversification. Herbivorous insects are classic models for ecological and evolutionary research, but it is recent advances in sequencing, statistics, and molecular technologies that have cleared the way for investigations into the proximate genetic mechanisms underlying host shifts. In this review, we discuss how genome-scale data are revealing-at resolutions previously unimaginable-the genetic architecture of host-use traits, the causal loci underlying host shifts, and the predictability of host-use evolution. Collectively, these studies are providing novel insights into longstanding questions about host-use evolution. On the basis of this synthesis, we suggest that different host-use traits are likely to differ in their genetic architecture (number of causal loci and the nature of their genetic correlations) and genetic predictability (extent of gene or mutation reuse), indicating that any conclusions about the causes and consequences of host-use evolution will depend heavily on which host-use traits are investigated. To draw robust conclusions and identify general patterns in host-use evolution, we argue that investigation of diverse host-use traits and identification of causal genes and mutations should be the top priorities for future studies on the evolutionary genetics of host shifts.

The predictability of genomic changes underlying a recent host shift in Melissa blue butterflies

“…Beyond host use in herbivorous insects, a limited number of studies have tried to predict genome‐wide patterns of genetic differentiation in nature from laboratory or field experiments, and mostly, these have involved predicting genetic differentiation from QTL studies. The outlier loci underlying highest genetic differentiation between Drosophila yakuba mainland (Cameroon and Kenya) and Mayotte populations show concordance with Drosophila sechellia noni‐tolerance (performance) QTL (four of nine tolerance QTL, expected = 0.125, p = .013), but there is no overlap for D. sechellia preference QTL (expected = 0.35, p = .37), suggesting that noni‐performance is more predictable than noni‐preference (Vertacnik & Linnen, ; Yassin et al., ). Similarly, QTL for ecologically relevant traits colocalized with possible genetic regions affected by selection (as identified in genome scans) more than expected by chance in comparison with lake whitefish ecotypes (Rogers & Bernatchez, ).…”

The predictability of genomic changes underlying a recent host shift in Melissa blue butterflies

“…Beyond host-use in herbivorous insects, a limited number of studies have tried to predict genome-wide patterns of genetic differentiation in nature from lab or field experiments, and mostly these have involved predicting genetic differentiation from QTL studies. The outlier loci underlying highest genetic differentiation between Drosophila yakuba mainland (Cameroon and Kenya) and Mayotte populations, show concordance with Drosophila sechellia noni-tolerance (performance) QTLs (four of nine tolerance QTL, expected = 0.125, P = 0.013) but there is no overlap for D. sechellia preference QTLs (expected = 0.35, P = 0.37), suggesting that noni-performance is more predictable than noni preference (Yassin et al, 2016; Vertacnik & Linnen, 2017). Similarly, QTL for ecologically relevant traits co-localized with possible genetic regions affected by selection (as identified in genome scans) more than expected by chance in comparisons of lake whitefish ecotypes (Rogers & Bernatchez, 2007).…”

Evaluating species interactions as a driver of phytophagous insect divergence

“…Considering that even species breeding on decaying and thus undefended tissues show this pattern, it is unlikely that coevolution and adaptation to plant defenses is a universal source of divergent selection and a necessary condition to explain insect diversification. A recent review found that most studies on candidate genes for host adaptation in phytophagous insects focus on resistance or detoxification of plant secondary metabolites [82], but the actual source of selection might be in other aspects of host use. Divergence following host shifts is pervasive in phytophagous insects and their parasitoids [26], despite the large variation in interaction outcomes.…”