A Novel Preference for an Invasive Plant as a Mechanism for Animal Hybrid Speciation

Abstract

Homoploid hybrid speciation-speciation via hybridization without a change in chromosome number-is rarely documented and poorly understood in animals. In particular, the mechanisms by which animal homoploid hybrid species become ecologically and reproductively isolated from their parents are hypothetical and remain largely untested by experiments. For the many host-specific parasites that mate on their host, choosing the right host is the most important ecological and reproductive barrier between these species. One example of a host-specific parasite is the Lonicera fly, a population of tephritid fruit flies that evolved within the last 250 years likely by hybridization between two native Rhagoletis species following a host shift to invasive honeysuckle. We studied the host preference of the Lonicera fly and its putative parent species in laboratory experiments. The Lonicera fly prefers its new host, introduced honeysuckle, over the hosts of both parental species, demonstrating the rapid acquisition of preference for a new host as a means of behavioral isolation from the parent species. The parent taxa discriminate against each other's native hosts, but both accept honeysuckle fruit, leaving the potential for asymmetric gene flow from the parent species. Importantly, this pattern allows us to formulate hypotheses about the initial formation of the Lonicera fly. As mating partners from the two parent taxa are more likely to meet on invasive honeysuckle than on their respective native hosts, independent acceptance of honeysuckle by both parents likely preceded hybridization. We propose that invasive honeysuckle served as a catalyst for the local breakdown of reproductive isolation between the native parent species, a novel consequence of the introduction of an exotic weed. We describe behavioral mechanisms that explain the initial hybridization and subsequent reproductive isolation of the hybrid Lonicera fly.These results provide experimental support for a combination of host shift and hybridization as a model for hybrid speciation in parasitic animals.

Host plant toxicity affects developmental rates in a polyphagous fruit fly: experimental evidence

“…Various, non-exclusive mechanisms have been invoked to explain the association between patterns of speciation and host plant use in phytophagous insects, such as shifts in (or expansion of) host plant use (Weingartner, Wahlberg & Nylin, 2006), hybridization (Schwarz et al, 2007), adaptive radiation (Braby & Trueman, 2006), specialization, and reproductive isolation (Schluter, 1998). A well-documented example of sympatric speciation associated with host plant use is provided by the monophagous apple maggot fly Rhagoletis pomonella (Walsh, 1867) (Diptera: Tephritidae) (Bush, 1969;Berlocher, 1998).…”

Are the ecological impacts of alien species misrepresented? A review of the “native good, alien bad” philosophy

“…The more intense a new interaction is, the more likely an adaptive response is to occur (providing that the 296 native species has a population that is large enough, and that has sufficient genetic variation, for this to occur). Well-studied examples of alien-influenced contemporary evolution are the genetic-based increase in toxin resistance in the native amphibian-eating red-bellied black snake ( (Schwarz et al 2007). This represents a rare example of homoploid hybrid speciation in animal taxa as a direct result of the introduction of a novel host species into the native community.…”

A genomic view of introgression and hybrid speciation

“…Here, success depends on the fixation of favourable new gene combinations from the two species [48]. For example, there are suggestions that new hybrid gene combinations facilitated critical ecological changes in several recently proposed hybrid species, including sculpins [49], Rhagoletis flies [50], and butterflies [51,52*]. In these cases, species of hybrid origin have colonized novel habitats, most likely through the expression of transgressive traits.…”