Does reproductive isolation evolve faster in larger populations via sexually antagonistic coevolution?

Sexual conflict over reproductive investment can lead to sexually antagonistic coevolution and reproductive isolation. It has been suggested that, unlike most models of allopatric speciation, the evolution of reproductive isolation through sexually antagonistic coevolution will occur faster in large populations as these harbour greater levels of standing genetic variation, receive larger numbers of mutations and experience more intense sexual selection. We tested this in bruchid beetle populations (Callosobruchus maculatus) by manipulating population size and standing genetic variability in replicated lines derived from founders that had been released from sexual conflict for 90 generations. We found that after 19 generations of reintroduced sexual conflict, none of our treatments had evolved significant overall reproductive isolation among replicate lines. However, as predicted, measures of reproductive isolation tended to be greater among larger populations. We discuss our methodology, arguing that reproductive isolation is best examined by performing a matrix of allopatric and sympatric crosses whereas measurement of divergence requires crosses with a tester line.     

Geographic variation in genital morphology of Ciulfina praying mantids

Geographic variation in morphological traits is widespread and important to our current understanding of evolutionary processes. Although male genitalia are perhaps the most divergent morphological traits in animals, geographic variation in genital traits has received little attention and the mechanism driving such variation is unclear. The species isolation hypothesis of genital evolution makes explicit predictions about geographic variation in genitalia predicting patterns of genital divergence that reflect the risk of mating with related but incompatible species. The sexual selection and pleiotropy hypotheses, however, predict general levels of geographic variation that reflect divergent sexual selection pressures or genetic drift. To test these predictions, we investigated geographic variation in genital morphology in the praying mantid genus Ciulfina (Mantodea: Liturgusidae) using elliptic Fourier analysis. We found significant levels of geographic variation in the genital morphology of four Ciulfina species irrespective of the relative proximity of different populations to contact zones with other species. These results reject the species isolation hypothesis, and instead support either the sexual selection or pleiotropy hypotheses to explain patterns of genital evolution in this genus.     

SPECIATION BY REINFORCEMENT OF PREMATING ISOLATION

The generation of premating isolation given partial or complete postzygotic isolation between populations is termed reinforcement or, in the case of complete isolation, reproductive character displacement. In this study we use computer simulations and a multilocus genetic model to reevaluate the theory of reinforcement. We consider the evolution of female preferences for a male secondary sexual trait. If the populations differ in mean female preference, there is direct selection on the preference for further divergence, which may be augmented by a correlated response to sexual selection on males. Two factors prevent divergence. First, if postzygotic isolation is not complete, gene flow can prevent divergence and lead to a hybrid swarm. This is the usual outcome whenever the average number of breeding adult offspring produced by a hybrid mating is sufficient to replace the parents. Second, one or the other population may become extinct because of the large number of hybrid matings it is involved in. The likelihood of extinction is lowered if population growth rates are high, if hybrids are inviable rather than infertile, or under some conditions when allopatric populations provide immigrants into the contact zone. Provided hybrid fitness is sufficiently low, there is a wide range of genetic and ecological conditions under which reinforcement rather easily occurs, and also a range under which it may occur because of stochastic effects on both the inheritance parameters and the population sizes.     

Are you more than the sum of your parents’ genes? Phenotypic plasticity in a clonal vertebrate and F1 hybrids of its parental species

All known vertebrate clones have originated from hybridization events and some have produced distinct evolutionary lineages via hybrid speciation. Amazon mollies (Poecilia formosa) present an excellent study system to investigate how clonal species have adapted to heterogeneous environments because they are the product of a single hybridization event between male sailfin mollies (Poecilia latipinna) and female Atlantic mollies (Poecilia mexicana). Here, we ask whether the hybrid species differs from the combination of its parental species’ genes in its plastic response to different environments. Using a three-way factorial design, we exposed neonates produced by Amazon mollies and reciprocal F1 hybrid crosses to different thermal (24°C and 29°C) and salinity (0/2, 12, and 20 ppt) regimes. We measured various ontogenetic and life history characteristics across the life span of females. Our major results were as follows: (1) Reaction norms of growth and maturation to temperature and salinity are quite similar between the two hybrid crosses; (2) Amazon molly reaction norms were qualitatively different than the P. latipinna male and P. mexicana female (L×M) hybrids for the ontogenetic variables; (3) Amazon molly reaction norms in reproductive traits were also quite different from L×M hybrids; and (4) The reaction norms of net fertility were very different between Amazon mollies and L×M hybrids. We conclude that best locale for Amazon mollies is not the best locale for hybrids, which suggests that Amazon mollies are not just an unmodified mix of parental genes but instead have adapted to the variable environments in which they are found. Hybridization resulting in asexuality may represent an underappreciated mechanism of speciation because the unlikely events required to produce such hybrids rarely occur and is dependent upon the genetic distance between parental species.     

INCIPIENT REPRODUCTIVE ISOLATION BETWEEN TWO SYMPATRIC MORPHS OF THE INTERTIDAL SNAIL LITTORINA SAXATILIS

The study of speciation in recent populations is essentially a study of the evolution of reproductive isolation mechanisms between sub-groups of a species. Prezygotic isolation can be of central importance to models of speciation, either being a consequence of reinforcement of assortative mating in hybrid zones, or a pleiotropic effect of morphological or behavioral adaptation to different environments. To suggest speciation by reinforcement between incipient species one must at least know that gene flow occurs, or have recently occurred, and that assortative mating has been established in the hybrid zone. In Galician populations of the marine snail Littorina saxatilis, two main morphs appear on the same shores, one on the upper-shore barnacle belt and the other in the lower-shore mussel belt. The two morphs overlap in distribution in the midshore where hybrids are found together with pure forms. Allozyme variation indicates that the two parental morphs share a common gene pool, although within shores, gene flow between morphs is less than gene flow within morphs. In this study, we observed mating behavior in the field, and we found that mating was not random in midshore sites, with a deficiency of heterotypic pairs. Habitat selection, assortative mating, and possibly sexual selection among females contributed to the partial reproductive isolation between the pure morphs. Sizes of mates were often positively correlated, in particular, in the upper shore, indicating size-assortative mating too. However, this seemed to be a consequence of nonrandom microdistributions of snails of different sizes. Because we also argue that the hybrid zone is of primary rather than secondary origin, this seems to be an example of sympatric reproductive isolation, either established by means of reinforcement or as a by-product to divergent selection acting on other characters.     

Reproductive protein evolution within and between species: maintenance of divergent ZP3 alleles in Peromyscus

In a variety of animal taxa, proteins involved in reproduction evolve more rapidly than nonreproductive proteins. Most studies of reproductive protein evolution, however, focus on divergence between species, and little is known about differentiation among populations within a species. Here we investigate the molecular population genetics of the protein ZP3 within two Peromyscus species. ZP3 is an egg coat protein involved in primary binding of egg and sperm and is essential for fertilization. We find that amino acid polymorphism in the sperm-combining region of ZP3 is high relative to silent polymorphism in both species of Peromyscus . In addition, while there is geographical structure at a mitochondrial gene ( Cytb ), a nuclear gene ( Lcat ) and eight microsatellite loci, we find no evidence for geographical structure at Zp3 in Peromyscus truei . These patterns are consistent with the maintenance of ZP3 alleles by balancing selection, possibly due to sexual conflict or pathogen resistance. However, we do not find evidence that reinforcement promotes ZP3 diversification; allelic variation in P. truei is similar among populations, including populations allopatric and sympatric with sibling species. In fact, most alleles are present in all populations sampled across P. truei's range. While additional data are needed to identify the precise evolutionary forces responsible for sequence variation in ZP3, our results suggest that in Peromyscus , selection to maintain divergent alleles within species contributes to the pattern of rapid amino acid substitution observed among species.     

Intrinsic reproductive isolation between Trinidadian populations of the guppy, Poecilia reticulata

Although Trinidadian populations of the guppy, Poecilia reticulata, show considerable adaptive genetic differentiation, they have been assumed to show little or no reproductive isolation. We tested this assumption by crossing Caroni (Tacarigua River) and Oropuche (Oropuche R.) drainage populations from Trinidad's Northern Range, and by examining multiple aspects of reproductive compatibility in the F1, F2 and BC1 generations. In open-aquarium experiments, F1 males performed fewer numbers of mating behaviours relative to parental population controls. This is the first documentation of hybrid behavioural sterility within a species, and it suggests that such sterility may feasibly be involved in causing speciation. The crosses also uncovered hybrid breakdown for embryo viability, brood size and sperm counts. In contrast, no reductions in female fertility were detected, indicating that guppies obey Haldane's rule for sterility. Intrinsic isolation currently presents a much stronger obstacle to gene flow than behavioural isolation, and our results indicate that Trinidadian populations constitute a useful model for investigating incipient speciation.