Sympatric Speciation in Phytophagous Insects: Moving Beyond Controversy?

Abstract

Sympatric speciation is the splitting of one evolutionary lineage into two without the occurrence of geographic isolation. The concept has been intimately tied to entomology since the 1860s, when Benjamin Walsh proposed that many host-specific phytophagous insects originate by shifting and adapting to new host plant species. If true, sympatric speciation would have tremendous implications for our understanding of species and their origins, biodiversity (25-40% of all animals are thought to be phytophagous specialists), insect-plant coevolution, community ecology, phylogenetics, and systematics, as well as practical significance for the management of insect pests. During much of the twentieth century sympatric speciation was viewed as much less plausible than geographic (allopatric) speciation. However, empirical field studies, laboratory experiments, developments in population genetics theory, and phylogenetic and biogeographic data have all recently combined to shed a more favorable light on the process. We review the evidence for sympatric speciation via host shifting for phytophagous insects and propose a set of testable predictions for distinguishing geographic mode (allopatric versus sympatric) of divergence. Our conclusion is that sympatric speciation is a viable hypothesis. We highlight areas where more thorough testing is needed to move sympatric speciation into the realm of accepted scientific theory.

Host-associated genetic structure of Mexican populations of the cabbage aphid Brevicoryne brassicae L. (Homoptera: Aphididae)

“…Genetic differentiation and restricted gene flow between host-associated populations may promote local adaptation in phytophagous insects (Berlocher and Feder, 2002). Ample evidence of host plant differentiation has recently been found in other aphids (eg De Barro et al, 1995a, b;Sunnucks et al, 1997;Via, 1999;Lushai et al, 2002), supporting the view that this phenomenon is much more widespread than previously realized.…”

“…If the host plant species constitute different selective environments to herbivorous insects, adaptive genetic differentiation among populations could arise (eg Rausher, 1984;Futuyma and Peterson, 1985;Mopper and Strauss, 1998). Local genetic differentiation of insect populations in relation to different host plants has been suggested as being an incipient stage of sympatric speciation and an important phenomenon maintaining genetic diversity in insects (Bush, 1994;Berlocher and Feder, 2002;Drès and Mallet, 2002).…”

Non-random gene flow: an underappreciated force in evolution and ecology

“…Habitat preferences can be controlled by genes affecting the physiological capacity of an organism to detect habitat cues, or its neurological ability to orient towards such cues. For instance, many phytophagous insects exhibit preferences for (or aversions to) the scent of particular host plants (reviewed in [30,31]). Such preferences sometimes coincide with higher performance in the preferred habitat [32] (see also Figure 1) but, in other cases, preference and performance are decoupled (e.g., [33][34][35]).…”

“…mating and allowing genetic divergence to build up between populations just tens of meters apart [15]. Habitat imprinting and host plant preferences are also widely invoked to explain speciation in phytophagous insects [31,67]. Thus, the degree to which gene flow and dispersal are random might substantially affect the speed and geographic context of speciation.…”

Evolutionary consequences of a search image

“…This is analogous to an extreme form of food imprinting, where a predator's prey preference is determined by its diet at a young age (Burghardt and Hess, 1966;Punzo, 2002). Imprinting as such could lead to speciation in the predator, because the predator starts to adapt specifically to the prey it is specialising on (see Via, 2001;Berlocher and Feder, 2002, for reviews on this issue). As such the formation of a search image in a predator could lead to different predator species evolving.…”