Have Genetic Trade-Offs in Host Use been Overlooked in Arthropods?

Abstract

A popular hypothesis to explain the high degree of host specialisation observed among mites and insects is the existence of host-associated fitness trade-offs. According to this theory, adaptation to a host results in a relatively poorer performance on alternative hosts due to the antagonistic pleiotropic action of one or more genes. Evidence in favour of the genetic trade-off hypothesis is however scarce. Recent ecological work has shown that the optimisation of adult performance drives the evolution of host choice in at least some phytophagous insects. Yet, most ecological and evolutionary studies on host choice assume that females maximise their fitness by optimising offspring performance. In this paper, we investigate whether a general lack of attention for the role of adult performance in host choice may have diminished the chance of detecting genetic trade-offs. We reviewed the literature on genetic trade-offs and showed that most studies neglected host specific variation in adult performance. Moreover, studies that considered both adult and offspring performance had a higher chance of detecting genetic fitness trade-offs. Our results also suggested that studies on asexual reproducing species tend to detect trade-offs more often than studies on obligate sexual reproducing species. We argue that future studies on genetic trade-offs should take all fitness parameters into account in order to be conclusive. This approach may reveal (i) that genetic trade-offs are more common than hitherto reported and/or (ii) that genetic trade-offs are more common, or more easily detected among asexual reproducing species like mites and aphids.

Niche explosion

“…Many attempts to identify such tradeoffs have failed, often finding that the generalist has high fitness and high performance across multiple hosts (Futuyma and Moreno 1988;Jaenike 1990;Scheirs et al 2005;Agosta and Klemens 2009). The lack of trade-offs is consistent with niche explosion hypothesis.…”

A Locus in Drosophila sechellia Affecting Tolerance of a Host Plant Toxin

“…These species prefer to oviposit and feed on host plants best suited for adult performance. As Scheirs et al (2005) point out, several studies that only consider larval performance also suggest that adult performance may have been affected by host quality (e.g., Karowe 1990;Herr and Johnson 1992;Lu and Logan 1994). Because adult D. sechellia tend to feed on fresh M. citrifolia (Tsacas and Bachli 1981), which can be toxic even to D. sechellia larvae (Rkha et al 1991), we believe that adult performance, rather than larval, is a key component of this adaptation.…”

“…Adult foraging is important in host preference for some phytophagous insect species, such as the grass miner Chromatomyia nigra (Scheirs et al 2005), the chrysomelid Altica carduorum (Scheirs et al 2005), and L. trifolii (Scheirs et al 2005). These species prefer to oviposit and feed on host plants best suited for adult performance.…”

“…Adapting to a new host can drive genetic and phenotypic change that is critical for isolating nascent species. In some cases, specialization has a price: Increased performance on the new host correlates with reduced performance on other hosts (Futuyma and Moreno 1988;Jaenike 1990;Fry et al 1996;Scheirs et al 2005; Via and Hawthorne 2005). This scenario poses a new challenge for the nascent specialist, as it must keep together alleles for finding and selecting the appropriate host ("preference") along with those for utilizing that host ("performance," e.g., physiologically adapting to that host's secondary compounds or nutritional content; Jaenike 1990; Janz 2011).…”

Macroevolution and the biological diversity of plants and herbivores

“…14 and 15), studies of host-plant-associated speciation (16)(17)(18), and especially quantitative genetic approaches to the question of whether or not tradeoffs exist in adaptation to different host plants. The latter approach is the dominant hypothesis to explain the prevalence of specialized host associations (19,20).…”