Genetic differentiation in the viability of sibling species of Rhagoletis fruit flies on host plants, and the influence of reduced hybrid viability on reproductive isolation

Prior theoretical studies have analyzed host-associated factors restricting gene flow between phytophagous insect species, and simulated evolutionary changes in components of fitness contributing to the adaptation of species to distinct host plants. However, there is relatively little empirical information on these topics. In this paper we report data on two host-associated sibling species of tephritid fruit flies, Rhagoletis mendax (Curran) and R. pomonella (Walsh) which infest ericaceous and rosaceous host plants, respectively. To test the hypothesis that these species have evolved viability differences on alternate hosts which can contribute to the restriction of gene flow between them, we measured the larval-to-adult viability of R. mendax, R. pomonella and F1 interspecific hybrid progeny reared on naturally-growing, highbush blueberry (Vaccinium corymbosum L.) and apple (Malus pumila Miller = Pyrus malus L.) plants in the field. Our results indicate that genetic changes associated with the adaptation of these species to distinct host plants could also cause reduced fitness of interspecific hybrids, and thereby restrict interspecific gene flow. Fewer interspecific hybrids survived to adulthood than either R. pomonella progeny reared in apples or R. mendax progeny reared in blueberries. These differences in the viability of progeny from hybrid versus conspecific crosses can substantially restrict gene flow between R. mendax and R. pomonella flies, and may be an important factor influencing their reproductive isolation. Genetic differences among hybrid and conspecific crosses were also detected for the lengths, widths and weights of pupae reared from blueberries and apples. In a second experiment, the ovipositional preferences of R. mendax and R. pomonella flies were recorded on host plants inside a field cage. R. mendax flies had a strong ovipositional preference for blueberries over apples, whereas R. pomonella flies readily oviposited in both host fruits. Other studies have determined that R. pomonella flies also oviposit in the fruits of several other plants which are not hosts under field conditions; this behavior can promote host shifts to new plants by flies with suitable plant-finding and viability traits. Our results support the theoretical assumption that divergence in host-acceptance behaviors and viabilities on host plants are key aspects of evolutionary differentiation among closely-related taxa of phytophagous parasitic insects. We discuss our results in the context of other traits that can restrict gene flow between R. mendax and R. pomonella, and in relation to the findings of other studies on the evolution of host plant use. Resume Differentiation evolutive d'especes jumelles de Rhagoletis: selection de la plante-hote par les adultes et survie des immatures Bien que des etudes theoriques aient analyse tant l'influence des elements de l'adaptabilite sur l'evolution de l'utilisation d'une plante par un insecte phytophage que les caracteristiques de l'hote limitant le flux genique entre especes voisines, peu de donnees concretes concernent ces aspects. Nos resultats portent sur deux especes jumelles de tephritides, R. mendax Curran et R. pomonella Walsh qui vivent respectivement sur ericacees et rosacees. Pour verifier si des differences dans le comportement d'acceptation des hotes et dans leur survie sur des hotes alternatifs sont apparues chez ces especes jumelles, nous avons observe dans la nature le comportement de ponte et la survie des 2 especes et des F1 hybrides interspecifiques sur Vaccinium corymbosum L. et Malus pumila Miller = Pyrus mali L. Le pourcentage de pondeuses, le nombre d'œufs pondus par femelle et la survie des larves ont ete plus eleves pour R. mendax que pour R. pomonella sur V. corymbosum, tandis que le contraire etait observe sur M. pumila. Des differences genetiques ont ete observees pour la mortalite avant la nymphose et avant La mue imaginale lors des croisements hybrides et interspecifiques. Les descendants mâles et femelles de R. mendax ont mieux survecu sur V. corymbosum, tandis que la survie de la descendance des croisements entre R. pomonella etait la meme sur les deux plantes. Un peu plus d'hybrides ont atteint le stade adulte sur pomme que de descendants de croisements intraspecifiques, et la mortalite des descendants de femelles de R. pomonella sur V. corymbosum etait plus elevee que celle des femelles de R. mendax. Les differences de survie et de comportement de ponte de R. mendax et de R. pomonella peuvent limiter le flux genique entre les 2 especes. Des differences genetiques peuvent etre observees quant a la taille et au poids des pupes de R. mendax et R. pomonella, Ces resultats confortent l'hypothese que des divergences evolutives du comportement d'acceptation de l'hote et de mortalite sur hotes respectifs sont des facteurs cles separant des taxa tres voisins d'insectes parasites phytophages. La discussion integre les autres aspects pouvant limiter le flux genique entre R. mendax et R. pomonella et les autres hypotheses sur l'evolution de l'exploitation des plantes hotes.