Body size differences do not arise from divergent mate preferences in a species pair of threespine stickleback

Ecological speciation can be driven by divergent natural and/or sexual selection. The relative contribution of these processes to species divergence, however, is unknown. Here, we investigate how sexual selection in the form of male and female mate preferences contributes to divergence of body size. This trait is known be under divergent natural selection and also contributes to sexual isolation in species pairs of threespine sticklebacks (Gasterosteus aculeatus). We show that neither female nor male size preferences contribute to body size divergence in this species pair, suggesting that size-based sexual isolation arises primarily through natural selection.     

Testing Wallace's intuition: water type,reproductive isolation and divergence in an Amazonian fish

Alfred Russel Wallace proposed classifying Amazon rivers based on their colour and clarity: white, black and clear water. Wallace also proposed that black waters could mediate diversification and yield distinct fish species. Here, we bring evidence of speciation mediated by water type in the sailfin tetra (Crenuchus spilurus), a fish whose range encompasses rivers of very distinct hydrochemical conditions. Distribution of the two main lineages concords with Wallace's water types: one restricted to the acidic and nutrient‐poor waters of the Negro River (herein Rio Negro lineage) and a second widespread throughout the remaining of the species’ distribution (herein Amazonas lineage). These lineages occur over a very broad geographical range, suggesting that despite occurring in regions separated by thousands of kilometres, individuals of the distinct lineages fail to occupy each other's habitats, hundreds of metres apart and not separated by physical barrier. Reproductive isolation was assessed in isolated pairs exposed to black‐water conditions. All pairs with at least one individual of the lineage not native to black waters showed significantly lower spawning success, suggesting that the water type affected the fitness and contributed to reproductive isolation. Our results endorse Wallace's intuition and highlight the importance of ecological factors in shaping diversity of the Amazon fish fauna.     

Evolution of reproductive isolation in stickleback fish

To understand how new species form and what causes their collapse, we examined how reproductive isolation evolves during the speciation process, considering species pairs with little to extensive divergence, including a recently collapsed pair. We estimated many reproductive barriers in each of five sets of stickleback fish species pairs using our own data and decades of previous work. We found that the types of barriers important early in the speciation process differ from those important late. Two premating barriers—habitat and sexual isolation—evolve early in divergence and remain two of the strongest barriers throughout speciation. Premating isolation evolves before postmating isolation, and extrinsic isolation is far stronger than intrinsic. Completing speciation, however, may require postmating intrinsic incompatibilities. Reverse speciation in one species pair was characterized by significant loss of sexual isolation. We present estimates of barrier strengths before and after collapse of a species pair; such detail regarding the loss of isolation has never before been documented. Additionally, despite significant asymmetries in individual barriers, which can limit speciation, total isolation was essentially symmetric between species. Our study provides important insight into the order of barrier evolution and the relative importance of isolating barriers during speciation and tests fundamental predictions of ecological speciation.     

Sequential mate choice and sexual isolation in threespine stickleback species

Sequential mate choice strategies predict how females should alter their choosiness based on the availability of attractive males. There are many studies on sequential mate choice within species, but few have asked whether females apply these strategies to interactions between species and how these strategies may affect hybridization. We tested how previous interactions with conspecific and heterospecific males affect mate preference and sexual isolation in two threespine stickleback species (benthics and limnetics: Gasterosteus spp.). Consistent with previous work, we found that within species, stickleback females gauge male attractiveness relative to previously encountered males. If females extend these decision rules between species, we predicted that previous interactions with conspecifics should make heterospecifics less attractive, whereas interactions with heterospecifics should make conspecifics more attractive. However, females found heterospecifics less attractive after prior experience, largely independent of the species of male first encountered. Thus, sequential mate choice strategies are used within but not between species in sticklebacks. Further, learning from prior courtship interactions acts to enhance existing sexual isolation between species.     

Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma)

Abstract .Theory predicts that sexual (or behavioral) isolation will be the first form of reproductive isolation to evolve in lineages characterized by sexual selection. Here I directly compare the rate of evolution of sexual isolation with that of hybrid inviability in a diverse and sexually dimorphic genus of freshwater fish. The magnitude of both sexual isolation and hybrid inviability were quantified for multiple pairs of allopatric species. Rates of evolution were inferred by comparing genetic distances of these species pairs with the magnitude of each form of reproductive isolation: the slope of the regression of genetic distance on the magnitude of reproductive isolation represents the rate of evolution. Of the two forms of isolation, the magnitude of sexual isolation exhibited the steeper slope of regression, indicating that sexual isolation will tend to evolve to completion earlier than hybrid inviability, strictly as a by-product of evolution in geographically isolated populations. Additional evidence from the literature is used to qualitatively compare rates of evolution of sexual isolation with that of other forms of reproductive isolation. Preliminary comparisons support the prediction that sexual isolation will evolve more rapidly than other forms. Because Etheostoma is characterized by striking sexual dimorphism, these results are consistent with the hypothesis that sexual selection for exaggerated mate-recognition characters causes the relatively rapid evolution of sexual isolation.     

Cline coupling and uncoupling in a stickleback hybrid zone

Strong ecological selection on a genetic locus can maintain allele frequency differences between populations in different environments, even in the face of hybridization. When alleles at divergent loci come into tight linkage disequilibrium, selection acts on them as a unit and can significantly reduce gene flow. For populations interbreeding across a hybrid zone, linkage disequilibria between loci can force clines to share the same slopes and centers. However, strong ecological selection on a locus can also pull its cline away from the others, reducing linkage disequilibrium and weakening the barrier to gene flow. We looked for this “cline uncoupling” effect in a hybrid zone between stream resident and anadromous sticklebacks at two genes known to be under divergent natural selection (Eda and ATP1a1) and five morphological traits that repeatedly evolve in freshwater stickleback. These clines were all steep and located together at the top of the estuary, such that we found no evidence for cline uncoupling. However, we did not observe the stepped shape normally associated with steep concordant clines. It thus remains possible that these clines cluster together because their individual selection regimes are identical, but this would be very surprising given their diverse roles in osmoregulation, body armor, and swimming performance.     

Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population

Under laboratory conditions, female three-spined sticklebacks(Gasterosteus aculeatus L.) show a mating preference for intenselyred-colored males. We verified this female choice in the fieldby observing a freshwater stickleback population in its naturalhabitat. During the egg collection phase, individual courtingmales were localized with the aid of a dummy of a ripe female,caught and photographed under standardized conditions, and released.After males had stopped collecting eggs, we counted the numberof eggs in the nests. The more intense a male's red breedingcoloration, the more eggs he received. Simultaneous female choiceexperiments in the laboratory suggested that ripe females ofthis population preferred redder males. Breeding activitiesof the males in the field were clustered and seem to be synchronizedwithin clusters. At one of the breeding sites, more intensered males were in better physical condition, but this was notthe case at another site. Although several synchronized breedingcycles were observed, the majority of males seem to completeonly one breeding cycle.     

Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces, Gasterosteidae)

The pelvic girdle of Gasterosteus aculeatus is normally a complex and robust structure that varies moderately among and within populations, but in several populations it occurs as a vestigial series. Based on 14 Recent and fossil populations from North America and Scotland, three general patterns of intrapopulation variation of vestigial pelvic structures can be recognized. In most cases of pelvic reduction, the size and complexity of the pelvic girdle are reduced mostly by progressive truncation of distal structures, but two patterns of distal truncation occur. Paedomorphosis appears to play a role in all cases of pelvic reduction, but in a fossil assemblage and one extant population it accounts for most of the structural simplification.
Pelvic reduction in populations of Gasterosteus depends on an interaction between natural selection, which appears to determine whether or not pelvic reduction occurs, and phylogenetic constraint (especially developmental constraint), which strongly influences the form of pelvic vestiges. The empirical difficulty of discriminating between phylogenetic constraint and effects of natural selection, and the potential for phylogenetic constraint to produce homoplasy are discussed. Pelvic reduction apparently has been a recurrent phenomenon in Gasterosteus since at least the early Pliocene, but it has not resulted in evolution of a separate lineage of 'pelvicless' sticklebacks because such populations are restricted to lakes, which are ephemeral over evolutionary time. Rapid phyletic pelvic reduction coupled with selective extinction of populations with vestigial pelvic structures has resulted in phylogenetic stasis.     

The evolution of partial reproductive isolation as an adaptive optimum

Decades of theoretical work on the evolution of adaptive prezygotic isolation have led to an interesting finding—namely that stable partial reproductive isolation is a relatively common outcome. This conclusion is generally lost, however, in the desire to pinpoint when exactly speciation occurs. Here, we argue that the evolution of partial reproductive isolation is of great interest in its own right and matches empirical findings that ongoing hybridization is taxonomically widespread. We present the mechanisms by which partial reproductive isolation can be a stable evolutionary endpoint, concentrating on insights from theoretical studies. We focus not on cases in which hybridization results from constraints imposed by ongoing migration or mutation, but on the intriguing idea that partial reproductive isolation may instead be an adaptive optimum. We identify three general categories of selective mechanisms that can lead to partial reproductive isolation: context-dependent hybrid advantage, indirect selection due to the varying actions of sexual selection in different geographic contexts, and a balance of costs of choosiness with indirect selection for stronger mating preferences. By any of these mechanisms, stable partial reproductive isolation can potentially provide a robust evolutionary alternative to either complete speciation or population fusion.     

Effects of Schistocephalus solidus (Cestoda) on the food intake and diet of the three-spined stickleback, Gasterosteus aculeatus

Seasonal differences were detected between uninfected sticklebacks and those infected with Schistocephalus solidus in their stomach fullness and diet composition.     

Evaluation of ovum fixation and storage in three-spined stickleback

Ripe eggs removed from three-spined sticklebacks stored in 50% isopropyl alcohol showed significantly Sower mean masses than those stored in 10% formalin. These results are considered in relationship to preservation techniques for stickleback.     

Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites

To assess the population genetic structure of the three-spined stickleback, Gasterosteus aculeatus, variability at 18 microsatellite loci was examined in 1724 individuals from 74 locations covering most of the species distribution range in Europe. The results revealed high overall degree of differentiation (F(ST) = 0.21) but contrasting level of divergence and genetic variability between habitat types. Marine populations were genetically relatively uniform even across great geographical distances as compared to substantial differentiation among freshwater populations. Analysis of molecular variance indicated low but significant (2.7%) variation in allele frequencies between geographical regions, but a negligible effect of habitat type (0.2%). The phylogenetic pattern was not explained by habitat type, but a weak signal of populations clustering according to geographical or water system origin was found. The results support the view that three-spined stickleback marine ancestors colonized northern European fresh waters during the postglacial marine submergence c. 10,000 years ago, whereas in the Mediterranean region colonization probably dates back to the Pleistocene. The independent origins of river and lake populations indicate that they originate from multiple colonizations rather than sharing common ancestry. In the continuous marine environment, the low degree of differentiation among populations can be explained by gene flow among subpopulations and large effective population size buffering divergence in neutral markers. In contrast, among postglacially established freshwater populations differentiation appears to be driven by genetic drift and isolation. The stepwise mutations appear to have contributed to the population differentiation in the southern part of the three-spined stickleback distribution range.     

How feeding performance and energy intake change with a small increase in the body size of the three-spined stickleback

Changes in the foraging behaviour due to variation in the body size of the three-spined stickleback Gasterosteus aculeatus were investigated. All sizes of fish had a high probability of attacking prey whenever encountered. The probability of eating the prey increased with the size of the fish, as the larger fish had larger jaws and a greater stomach capacity. Therefore, as fish increased in size there was an increase in the probability of successful prey capture. The level of satiation did not have an effect on the prey handling time, which is contrary to other studies and is probably a result of the large prey sizes. The physical size of the prey meant that the handling times were long regardless of the motivational level of the fish. The larger fish took in more energy and at a faster rate, although the time to reach satiation was similar for all fish sizes. The advantage that large fish appear to have in successfully gaining large prey is negated by their greater metabolic requirement. The changes in feeding performance induced by small increases in body size could have important consequences for intraspecific competition, habitat Use and risk of predation.     

Sexual conflict and reproductive isolation in flies

Sexual conflict is predicted to generate more rapid reproductive isolation between larger populations. While there is some empirical support for this, the data are inconsistent and, additionally, there has been criticism of some of the evidence. Here we reanalyse two experimental-evolution datasets using an isolation index widely applied in the speciation literature. We find evidence for reproductive isolation through sexual conflict in Sepsis cynipsea, but not in Drosophila melanogaster, and this occurred to a greater degree in larger populations, which is consistent with previous findings.     

Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity

The goal of this study was to evaluate the role of common ancestry, and of geographical or reproductive isolation, in genetic divergence in populations of threespine sticklebacks (Gasterosteus aculeatus). Using seven DNA microsatellite loci we compared the effects of habitat type, drainage system and geographical proximity on genetic distance among 16 populations situated in an area in Schleswig-Holstein (Germany) that became deglaciated approximately 12 000 years ago. Stickleback population structure correlated only weakly with drainage system, whereas the primary divergence was among habitat types. Phylogenetic analysis revealed that lake (n = 7) and river (n = 5) populations formed two distinct clades (Cavalli-Sforza's and Edwards' chord distance, 82-100% bootstrap support) at approximately equal genetic distances to a third clade, comprising putative estuarine (n = 4) ancestors. Allele frequencies in lake and river populations represented different subsets of the genetically more diverse estuarine populations. In nested amovas approximately twice the genetic variance was distributed among lake vs. river vs. estuarine populations as compared with the combined effects of drainage system and geographical distance. Limited gene flow between habitat types must have been established after postglacial colonization, suggesting ecological hybrid inferiority or behavioural mating barriers between ecotypes. Within estuarine and lake populations, population differentiation followed an isolation-by-distance model. Given the high observed heterozygosities within the 16 study populations (HO = 0.65-0.87), the mean divergence between lake and river population pairs (FST = 0.18 +/- 0.007) would be reached after 300-6000 generations in a stepwise mutation model, depending on the size of N(e). This demonstrates both the utility of hypervariable microsatellites for detecting recent population divergences and the danger of operating at temporal or spatial scales which are beyond their resolution.     

Parallels,nonparallels, and plasticity in population differentiation of threespine stickleback within a lake

The frequent occurrence of parallel phenotypic divergence in similar habitats is often evoked when emphasizing the role of ecology in adaptive radiation and speciation. However, because phenotypic plasticity can contribute to the observed pattern of divergence, confirmation of divergence at loci underlying phenotypic traits is important for confirming adaptive divergence. In the present study, we examine parallel morphological, neutral, and potentially adaptive genetic divergence of threespine stickleback inhabiting different habitats within a lake. Three genetic clusters best explained the neutral genetic structure within the lake; however, morphological differences were only weakly connected to genetic clusters and there was considerable phenotypic variation within clusters. Among the factors that could contribute to the observed pattern of morphological and genetic divergence are phenotypic plasticity, selective mortality of hybrids, and habitat choice based on morphology. Several loci are identified as outliers indicating divergent selection between the morphs and some parallels in morphological and adaptive genetic divergence are found in stickleback spawning at two lava sites. However, neutral genetic structure indicates considerable genetic connectivity among the two lava sites, and the parallels in morphology may therefore represent selective distribution of phenotypes rather than parallel divergence. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 803–813.     

The influence of prey size and abundance, and individual phenotype on prey choice by the three-spined stickleback, Gasterosteus aculeatm L.

Prey selection behaviour of three-spined sticklebacks, Gasterosteus aculeatus L., was studied in two experiments. Where possible, the experimental apparatus satisfied the assumptions of the simplest optimal diet model (the basic prey model); prey were presented sequentially, the fish could not search for and handle prey at the same time, and net energy gain, handling time and encounter rate were fixed. Experiment 1 presented fish with a range of Asellus sizes so that pursuit ( p ) and handling ( h ) time could be related to prey size. Published energy values of Asellus together with pursuit and handling times were used to calculate E /( p+h ) for Asellus measuring 3,4,5,6,7 and 9 mm. Pursuit times did not differ with prey size but handling times did. E /( p+h ) was very variable particularly at the larger prey sizes. Experiment 2 presented fish with two sequences of prey differing in the encounter rate with the most profitable prey sizes. Fish did not select the diet predicted by the basic prey model tending to always ignore the largest prey even when net energy gain would have been maximized by including them in the diet. Further analysis showed that the probability of a prey size being taken was a function of prey size, fish stomach fullness and encounter rate. It is concluded that the basic prey model is too simple to capture the behaviour of the fish. One of its main faults is that the changing state of the fish through the feeding bout is ignored.     

Assessing reproductive isolation using a contact zone between parapatric lake‐stream stickleback ecotypes

Ecological speciation occurs when populations evolve reproductive isolation as a result of divergent natural selection. This isolation can be influenced by many potential reproductive barriers, including selection against hybrids, selection against migrants and assortative mating. How and when these barriers act and interact in nature is understood for relatively few empirical systems. We used a mark–recapture experiment in a contact zone between lake and stream three‐spined sticklebacks (Gasterosteus aculeatus, Linnaeus) to evaluate the occurrence of hybrids (allowing inferences about mating isolation), the interannual survival of hybrids (allowing inferences about selection against hybrids) and the shift in lake‐like vs. stream‐like characteristics (allowing inferences about selection against migrants). Genetic and morphological data suggest the occurrence of hybrids and no selection against hybrids in general, a result contradictory to a number of other studies of sticklebacks. However, we did find selection against more lake‐like individuals, suggesting a barrier to gene flow from the lake into the stream. Combined with previous work on this system, our results suggest that multiple (most weakly and often asymmetric) barriers must be combining to yield substantial restrictions on gene flow. This work provides evidence of a reproductive barrier in lake–stream sticklebacks and highlights the value of assessing multiple reproductive barriers in natural contexts.