Divergent adaptation promotes reproductive isolation among experimental populations of the filamentous fungus Neurospora

Abstract

BackgroundAn open, focal issue in evolutionary biology is how reproductive isolation and speciation are initiated; elucidation of mechanisms with empirical evidence has lagged behind theory. Under ecological speciation, reproductive isolation between populations is predicted to evolve incidentally as a by-product of adaptation to divergent environments. The increased genetic diversity associated with interspecific hybridization has also been theorized to promote the development of reproductive isolation among independent populations. Using the fungal model Neurospora, we founded experimental lineages from both intra- and interspecific crosses, and evolved them in one of two sub-optimal, selective environments. We then measured the influence that initial genetic diversity and the direction of selection (parallel versus divergent) had on the evolution of reproductive isolation.ResultsWhen assayed in the selective environment in which they were evolved, lineages typically had greater asexual fitness than the progenitors and the lineages that were evolved in the alternate, selective environment. Assays for reproductive isolation showed that matings between lineages that were adapted to the same environment had greater sexual reproductive success than matings between lineages that were adapted to different environments. Evidence of this differential reproductive success was observed at two stages of the sexual cycle. For one of the two observed incompatibility phenotypes, results from genetic analyses were consistent with a two-locus, two-allele model with asymmetric (gender-specific), antagonistic epistasis. The effects of divergent adaptation on reproductive isolation were more pronounced for populations with greater initial genetic variation.ConclusionDivergent selection resulted in divergent adaptation and environmental specialization, consistent with fixation of different alleles in different environments. When brought together by mating, these alleles interacted negatively and had detrimental effects on sexual reproductive success, in agreement with the Dobzhansky-Muller model of genetic incompatibilities. As predicted by ecological speciation, greater reproductive isolation was observed among divergent-adapted lineages than among parallel-adapted lineages. These results support that, given adequate standing genetic variation, divergent adaptation can indirectly cause the evolution of reproductive isolation, and eventually lead to speciation.

Morphological variation and reproductive incompatibility of three coconut-mite-associated populations of predatory mites identified as Neoseiulus paspalivorus (Acari: Phytoseiidae)

“…Moreover, reproductive isolation has been shown to represent an initial step in the speciation process by preventing or greatly reducing gene flow between populations (Laven 1959(Laven , 1967Conner and Saul 1986;Thompson 1987;Dettman et al 2008), and our data are therefore consistent with incipient allopatric speciation (Drès and Mallet 2002;Gavrilets 2003;Coyne and Orr 2005) among these three geographically isolated specimens identified as N. paspalivorus.…”

“…Taken together, we expect the reproductive incompatibility observed in this study, to be the result of genetic divergence due to allopatric differentiation among the populations investigated (Hurt and Hedrick 2003;Dettman et al 2008) rather than to be caused by Wolbachia. Even if endosymbionts would be present, there is no guarantee that they were the cause of reproductive isolation because some Wolbachia strains are incapable of inducing reproductive incompatibility in their host (Giordano et al 1995;Turrelli and Hoffmann 1995;Gotoh et al 2005).…”

“…Reproductive isolation is generally thought to develop by the gradual accumulation of genetic differences between populations as a by-product of other adaptive or neutral genetic changes that take place in allopatry (Mayr 1963;Charlesworth et al 1987;Coyne 1992Coyne , 1993Wu and Davis 1993;Drès and Mallet 2002;Gavrilets 2003;Coyne and Orr 2005;Dettman et al, 2008). Moreover, reproductive isolation has been shown to represent an initial step in the speciation process by preventing or greatly reducing gene flow between populations (Laven 1959(Laven , 1967Conner and Saul 1986;Thompson 1987;Dettman et al 2008), and our data are therefore consistent with incipient allopatric speciation (Drès and Mallet 2002;Gavrilets 2003;Coyne and Orr 2005) among these three geographically isolated specimens identified as N. paspalivorus.…”

The existence of species rests on a metastable equilibrium between inbreeding and outbreeding

“…In French, we have a proverb that says 'Ce qui se ressemble s'assemble', and the existence of races and varieties in the natural world vouches for the spontaneous occurrence of structuration of natural populations which can only be the result of some preferential association, and reproduction, between individuals that are more closely related to one another than to the rest of the population. The recent finding that, even in the fungus Neurospora, some degree of reproductive isolation could be observed between stocks that had been grown for relatively short periods in different selective environments [74] indicates that a tendency for preferential mating with individuals bearing similar phenotypes can occur even in microscopic organisms.…”

The roles of standing genetic variation and evolutionary history in determining the evolvability of anti-predator strategies

“…While an allele may be mildly deleterious or confer no fitness advantage over other forms under one set of environmental conditions [6], that allele may become beneficial if the environment changes. As selection can act only on available variation, SGV provides a potential means for more rapid adaptive evolution ( [7][8][9][10][11][12][13][14][15][16][17][18][19][20]; reviewed in [21]) compared with the de novo mutations [5,22], particularly if the environment changes (e.g. if a new predator or competitor invades the system, or if abiotic conditions change).…”