Asymmetrical Reinforcement and Wolbachia Infection in Drosophila

Abstract

Reinforcement refers to the evolution of increased mating discrimination against heterospecific individuals in zones of geographic overlap and can be considered a final stage in the speciation process. One the factors that may affect reinforcement is the degree to which hybrid matings result in the permanent loss of genes from a species' gene pool. Matings between females of Drosophila subquinaria and males of D. recens result in high levels of offspring mortality, due to interspecific cytoplasmic incompatibility caused by Wolbachia infection of D. recens. Such hybrid inviability is not manifested in matings between D. recens females and D. subquinaria males. Here we ask whether the asymmetrical hybrid inviability is associated with a corresponding asymmetry in the level of reinforcement. The geographic ranges of D. recens and D. subquinaria were found to overlap across a broad belt of boreal forest in central Canada. Females of D. subquinaria from the zone of sympatry exhibit much stronger levels of discrimination against males of D. recens than do females from allopatric populations. In contrast, such reproductive character displacement is not evident in D. recens, consistent with the expected effects of unidirectional cytoplasmic incompatibility. Furthermore, there is substantial behavioral isolation within D. subquinaria, because females from populations sympatric with D. recens discriminate against allopatric conspecific males, whereas females from populations allopatric with D. recens show no discrimination against any conspecific males. Patterns of general genetic differentiation among populations are not consistent with patterns of behavioral discrimination, which suggests that the behavioral isolation within D. subquinaria results from selection against mating with Wolbachia-infected D. recens. Interspecific cytoplasmic incompatibility may contribute not only to post-mating isolation, an effect already widely recognized, but also to reinforcement, particularly in the uninfected species. The resulting reproductive character displacement not only increases behavioral isolation from the Wolbachia-infected species, but may also lead to behavioral isolation between populations of the uninfected species. Given the widespread occurrence of Wolbachia among insects, it thus appears that there are multiple ways by which these endosymbionts may directly and indirectly contribute to reproductive isolation and speciation.

Reinforcement generates reproductive isolation between neighbouring conspecific populations of spadefoot toads

“…Indeed, if reinforcement occurs with different heterospecifics in different parts of a focal species's range, or in different ways across sympatry and allopatry, it can contribute to 'speciation cascades' in which multiple speciation events are triggered by reinforcement [1,8,13], a process that has also been called the 'cascade reinforcement hypothesis' and 'RCD speciation' [9,15,16,20] (see also [6]). That reinforcement can initiate speciation remains controversial [18,19], despite empirical and theoretical studies suggesting that it can contribute to population divergence and reproductive isolation [8,[10][11][12][13]17]. Our work highlights the possibility that reinforcement can not only initiate reproductive isolation between conspecific populations, but also that it can do so even among neighbouring populations that differ in exposure to heterospecifics with which mating is costly.…”

“…When interactions with heterospecifics are costly (as when hybridization results in offspring of low fitness), selection should favour behaviours that prevent reproductive interactions, thereby enhancing isolation between species (or incipient species) to the point where gene exchange between them is reduced or completely eliminated [3,36,38,39]. Yet reinforcement (and, more generally, reproductive character displacement) may also serve to initiate divergence-and possibly speciation [1,2,[6][7][8][9][10][11][12][13][14][15][16][17]43]. Indeed, if reinforcement occurs with different heterospecifics in different parts of a focal species's range, or in different ways across sympatry and allopatry, it can contribute to 'speciation cascades' in which multiple speciation events are triggered by reinforcement [1,8,13], a process that has also been called the 'cascade reinforcement hypothesis' and 'RCD speciation' [9,15,16,20] (see also [6]).…”

“…In particular, because selection to avoid heterospecifics acts only where heterospecifics are actually encountered, traits that evolve via reproductive character displacement in sympatry do not also evolve in allopatric populations. If such trait differences become sufficiently pronounced, individuals in sympatry or allopatry may fail to recognize members of the alternative population type as acceptable mates [8,11,12,17]. Conspecific populations in sympatry and allopatry could thereby become reproductively isolated, and, ultimately, speciation between them could occur [1,2,[6][7][8][9][10][11][12][13][14][15][16][17] (but see [18,19]).…”

Host genotype changes bidirectional to unidirectional cytoplasmic incompatibility in Nasonia longicornis

“…Some of the mechanisms by which Wolbachia achieve this are killing of infected males, induction of parthenogenesis in infected females, feminization of genetic males and cytoplasmic incompatibility (CI) (reviewed in Werren et al, 2008). As a result, Wolbachia-induced host-reproductive manipulation has profound implications for many fundamental biological processes, such as sex determination (Rigaud et al, 1997;Werren and Beukeboom, 1998), sexual selection (Jiggins et al, 2000;Koukou et al, 2006), speciation (Laven, 1959;Breeuwer and Werren, 1990;Bordenstein et al, 2001;Jaenike et al, 2006) and organization of host genome structure (Kondo et al, 2002b, Dunning-Hotopp et al, 2007.…”

Adaptive immunity in invertebrates: A straw house without a mechanistic foundation

“…They cannot therefore offer a general new concept that can be applied across a range of invertebrate taxa. (10) reproductive isolation, (11) a switch in life-history strategy, (12) or immune responses to infection. (13) Similarly there are a number of components which contribute to the virulence of any pathogen including the production of virulence factors, (14) quorum sensing interactions (15) and competition with homologous and heterologous parasites for limited host resources.…”