Competitive Reduction by Satyrization? Evidence for Interspecific Mating in Nature and Asymmetric Reproductive Competition between Invasive Mosquito Vectors

Abstract

Abstract. Upon mating, male mosquitoes transfer accessory gland proteins (Acps) that induce refractoriness to further mating in females. This can also occur because of cross-insemination by males of related species, a process known as mating interference (satyrization). This mechanism could explain the competitive displacement of resident Aedes aegypti by the invasive Aedes albopictus where they co-occur. We tested this hypothesis in mosquito populations in Florida. A new polymerase chain reaction species diagnostic applied to sperm dissected from 304 field-collected females revealed bidirectional cross-mating in five (1.6%) individuals. Cross-injections of females with Acps showed that Ae. albopictus males induced monogamy in heterospecific females but not Ae. aegypti males. Despite its low frequency in the areas under study, the first evidence of cross-mating in nature and the asymmetric effect of Acps on mating suggest that satyrization may have initially contributed to the observed competitive reduction of Ae. aegypti by invasive Ae. albopictus in many areas.

Evolution of resistance to satyrization through reproductive character displacement in populations of invasive dengue vectors

“…Following recent findings that A. aegypti and A. albopictus mate bidirectionally in sites of sympatry in Florida (14) and that heterospecific male accessory gland products render A. aegypti but not A. albopictus females refractory to further insemination by conspecific males (14), we here provide evidence that satyrization has led to reproductive character displacement of A. aegypti by A. albopictus. In particular, we compare the frequency of interspecific mating between A. aegypti and A. albopictus from sympatric and allopatric populations, that is, populations where the two species either have been exposed to interspecific mating in the field or have not yet come in contact.…”

“…Among the possible mechanisms, the most widely cited is larval resource competition (11,12). However, it is considered unlikely that larval competition alone could account for the rapid competitive reductions of A. aegypti within 1-3 y in the southeastern United States (7,13,14) or in Bermuda, where A. albopictus more recently displaced A. aegypti with comparable rapidity (15). In addition to larval competition, hypotheses to explain these displacements include greater reproductive efficiency in A. albopictus (16); apparent competition mediated by the intestinal gregarine protozoan Ascogregarina taiwanesis (12); and asymmetric reproductive interference between A. aegypti and A. albopictus (4,13).…”

Invasiveness ofAedes aegyptiandAedes albopictusand Vectorial Capacity for Chikungunya Virus

“…Interspecific matings between these species occur in nature wherever their ranges overlap but yield no offspring, and A. aegypti populations are affected more deleteriously by the errant matings than A. albopictus. This is because virgin female A. aegypti but not A. albopictus females are sterilized by accessory gland substances from heterospecific males [15]. Satyrization has been suggested to be an adaptation, or exaptation (a nonadaptive change), favoring the invasive success of A. albopictus [16].…”

“…Although the superiority of A. albopictus over A. aegypti in larval competition in resource-limited environments was formerly proposed as the most likely causal mechanism for observed displacements [5], recently a form of asymmetric reproductive interference, satyrization, has been proposed as a more likely cause of the rapid displacements and reductions of A. aegypti [15]. Interspecific matings between these species occur in nature wherever their ranges overlap but yield no offspring, and A. aegypti populations are affected more deleteriously by the errant matings than A. albopictus.…”

The Effects of Interspecific Courtship on the Mating Success ofAedes aegyptiandAedes albopictus(Diptera: Culicidae) Males

“…albopictus, refractory to further mating (Tripet et al 2011). This satyrizing effect may be a powerful mechanism (Ribeiro and Spielman 1986, Ribeiro 1988, Nasci et al 1989, Lounibos 2007, Tripet et al 2011, Bargielowski et al 2013, Bargielowski and Lounibos 2014 in the displacement of Ae. aegypti populations by invading Ae.…”