The evolution of life cycle complexity in aphids: Ecological optimization or historical constraint?

Abstract

For decades, biologists have debated why many parasites have obligate multihost life cycles. Here, we use comparative phylogenetic analyses of aphids to evaluate the roles of ecological optimization and historical constraint in the evolution of life cycle complexity. If life cycle complexity is adaptive, it should be evolutionarily labile, that is, change in response to selection. We provide evidence that this is true in some aphids (aphidines), but not others (nonaphidines)-groups that differ in the intensity of their relationships with primary hosts. Next, we test specific mechanisms by which life cycle complexity could be adaptive or a constraint. We find that among aphidines there is a strong association between complex life cycles and polyphagy but only a weak correlation between life cycle complexity and reproductive mode. In contrast, among nonaphidines the relationship between life cycle complexity and host breadth is weak but the association between complex life cycles and sexual reproduction is strong. Thus, although the adaptiveness of life cycle complexity appears to be lineage specific, across aphids, life cycle evolution appears to be tightly linked with the evolution of other important natural history traits.

Dynamic Acquisition and Loss of Dual-Obligate Symbionts in the Plant-Sap-Feeding Adelgidae (Hemiptera: Sternorrhyncha: Aphidoidea)

“…It is reasonable to hypothesize that a highly adaptive strategy might have multiple origins within Adelgidae. The same has been proposed for host-alternating aphids (von Dohlen and Moran, 2000; Jousselin et al, 2010; Hardy et al, 2015). …”

Phylogenetic analysis reveals positive correlations between adaptations to diverse hosts in a group of pathogen-like herbivores

“…Elucidating those constraints remains a challenge in most systems, but testing hypotheses about the long‐term evolutionary relationships between host‐related ecological traits is feasible with phylogenetic comparative methods (Hardy et al. ). We advocate this empirical, macroevolutionary viewpoint as a complementary approach to theoretical models and experimental tests of the factors influencing host use and the evolution of ecological specialization.…”

“…; Hardy et al. ). However, interpreting specialization in these and many other plant‐feeding insects is complicated by the fact that both host preference and performance influence realized host use (Forister et al.…”

“…Long-term evolutionary processes affecting host use can be investigated empirically through phylogenetic analysis, and researchers have used phylogenetic comparative methods to examine evolutionary patterns in host use in many plant-feeding insects, such as butterflies (Janz et al 2001;Hardy and Otto 2014), bark beetles (Kelley and Farrell 1998), leaf beetles (Futuyma et al 1995), and aphids (Jousselin et al 2010;Hardy et al 2015). However, interpreting specialization in these and many other plantfeeding insects is complicated by the fact that both host preference and performance influence realized host use (Forister et al 2012).…”

Polyphyly of the extinct family Oviparosiphidae and its implications for inferring aphid evolution (Hemiptera, Sternorrhyncha)

“…Despite the undoubted advantages, this approach also brings many challenges, especially for such a complex group as aphids, and it has been applied in a very limited way for studying aphid evolution, e.g. [16]. Although not very numerous, the Mesozoic fossils can provide very important data on the body structure at the early stages of aphid evolution, if they are carefully considered in phylogenetic context.…”