Assortative Mating in an Ecological Context: Effects of Mate Choice Errors and Relative Species Abundance on the Frequency and Asymmetry of Hybridization.

AbstractThe frequency and asymmetry of mixed-species mating set the initial stage for the ecological and evolutionary implications of hybridization. How such patterns of mixed-species mating, in turn, are influenced by the combination of mate choice errors and relative species abundance remains largely unknown. We develop a mathematical model that generates predictions for how relative species abundances and mate choice errors affect hybridization patterns. When mate choice errors are small (<5%), the highest frequency of hybridization occurs when one of the hybridizing species is at low abundance, but when mate choice errors are high (>5%), the highest hybridization frequency occurs when species occur in equal proportions. Furthermore, females of the less abundant species are overrepresented in mixed-species matings. We compare our theoretical predictions with empirical data on naturally hybridizing Ficedula flycatchers and find that hybridization is highest when the two species occur in equal abundance, implying rather high mate choice errors. We discuss ecological and evolutionary implications of our findings and encourage future work on hybrid zone dynamics that take demographic aspects, such as relative species abundance, into account.

Parallel shifts of visual sensitivity and body coloration in replicate populations of extremophile fish.

Visual sensitivity and body pigmentation are often shaped by both natural selection from the environment and sexual selection from mate choice. One way of quantifying the impact of the environment is by measuring how traits have changed after colonization of a novel habitat. To do this, we studied Poecilia mexicana populations that have repeatedly adapted to extreme sulphidic (H2 S-containing) environments. We measured visual sensitivity using opsin gene expression, as well as body pigmentation, for populations in four independent drainages. Both visual sensitivity and body pigmentation showed significant parallel shifts towards greater medium-wavelength sensitivity and reflectance in sulphidic populations. Altogether we found that sulphidic habitats select for differences in visual sensitivity and pigmentation. Shifts between habitats may be due to both differences in the water's spectral properties and correlated ecological changes.

Plasticity contributes to a fine-scale depth gradient in sticklebacks' visual system.

The light environment influences an animal's ability to forage, evade predators, and find mates, and consequently is known to drive local adaptation of visual systems. However, the light environment may also vary over fine spatial scales at which genetic adaptation is difficult. For instance, in aquatic systems, the available wavelengths of light change over a few metres depth. Do animals plastically adjust their visual system to such small-scale environmental light variation? Here, we show that in three-spine stickleback (Gasterosteus aculeatus), opsin gene expression (an important determinant of colour vision) changes over a 2-m vertical gradient in nest depth. By experimentally altering the light environment using light filters to cover enclosures in a lake, we found that opsin expression can be adjusted on a short time frame (weeks) in response to the local light environment. This is to our knowledge the smallest spatial scale on which visual adjustments through opsin expression have been recorded in a natural setting along a continuously changing light environment.

Rapid adaptive evolution of colour vision in the threespine stickleback radiation.

Vision is a sensory modality of fundamental importance for many animals, aiding in foraging, detection of predators and mate choice. Adaptation to local ambient light conditions is thought to be commonplace, and a match between spectral sensitivity and light spectrum is predicted. We use opsin gene expression to test for local adaptation and matching of spectral sensitivity in multiple independent lake populations of threespine stickleback populations derived since the last ice age from an ancestral marine form. We show that sensitivity across the visual spectrum is shifted repeatedly towards longer wavelengths in freshwater compared with the ancestral marine form. Laboratory rearing suggests that this shift is largely genetically based. Using a new metric, we found that the magnitude of shift in spectral sensitivity in each population corresponds strongly to the transition in the availability of different wavelengths of light between the marine and lake environments. We also found evidence of local adaptation by sympatric benthic and limnetic ecotypes to different light environments within lakes. Our findings indicate rapid parallel evolution of the visual system to altered light conditions. The changes have not, however, yielded a close matching of spectrum-wide sensitivity to wavelength availability, for reasons we discuss.

Intruder colour and light environment jointly determine how nesting male stickleback respond to simulated territorial intrusions.

Variation in male nuptial colour signals might be maintained by negative frequency-dependent selection. This can occur if males are more aggressive towards rivals with locally common colour phenotypes. To test this hypothesis, we introduced red or melanic three-dimensional printed-model males into the territories of nesting male stickleback from two optically distinct lakes with different coloured residents. Red-throated models were attacked more in the population with red males, while melanic models were attacked more in the melanic male lake. Aggression against red versus melanic models also varied across a depth gradient within each lake, implying that the local light environment also modulated the strength of negative frequency dependence acting on male nuptial colour.

Mandated data archiving greatly improves access to research data.

The data underlying scientific papers should be accessible to researchers both now and in the future, but how best can we ensure that these data are available? Here we examine the effectiveness of four approaches to data archiving: no stated archiving policy, recommending (but not requiring) archiving, and two versions of mandating data deposition at acceptance. We control for differences between data types by trying to obtain data from papers that use a single, widespread population genetic analysis, structure. At one extreme, we found that mandated data archiving policies that require the inclusion of a data availability statement in the manuscript improve the odds of finding the data online almost 1000-fold compared to having no policy. However, archiving rates at journals with less stringent policies were only very slightly higher than those with no policy at all. We also assessed the effectiveness of asking for data directly from authors and obtained over half of the requested datasets, albeit with ∼8 d delay and some disagreement with authors. Given the long-term benefits of data accessibility to the academic community, we believe that journal-based mandatory data archiving policies and mandatory data availability statements should be more widely adopted.

Unravelling migratory connections: the next level.

Migration is widespread among birds, and the strength of the link between the breeding and wintering grounds, migratory connectivity, influences many ecological and evolutionary processes. Despite its importance, migratory connectivity is poorly estimated for most species. Traditionally, visual observations and bird ringing have been used to monitor migration, but these methods require more effort for relatively little return. Genetic markers and stable isotope signatures have increasingly been used to study connectivity. Each approach has its distinct strengths and weaknesses, and as is often the case, a combination may yield the most insight. In this issue of Molecular Ecology, Rundel and colleagues (2013) present a novel Bayesian statistical framework in which genetics and stable isotope data can be combined to improve the assignment of individuals to different winter or breeding regions. The development of such new statistical methods combined with the increasing number and ease of access of isotopic and genetic data sets will greatly enhance our understanding of migratory connectivity. Add to this the developments of miniature devices to track movements of individuals, and the field is destined to make major progression in the decades to come.

Multiple post-mating barriers to hybridization in field crickets.

Mechanisms that prevent different species from interbreeding are fundamental to the maintenance of biodiversity. Barriers to interspecific matings, such as failure to recognize a potential mate, are often relatively easy to identify. Those occurring after mating, such as differences in the how successful sperm are in competition for fertilisations, are cryptic and have the potential to create selection on females to mate multiply as a defence against maladaptive hybridization. Cryptic advantages to conspecific sperm may be very widespread and have been identified based on the observations of higher paternity of conspecifics in several species. However, a relationship between the fate of sperm from two species within the female and paternity has never been demonstrated. We use competitive microsatellite PCR to show that in two hybridising cricket species, Gryllus bimaculatus and G. campestris, sequential cryptic reproductive barriers are present. In competition with heterospecifics, more sperm from conspecific males is stored by females. Additionally, sperm from conspecific males has a higher fertilisation probability. This reveals that conspecific sperm precedence can occur through processes fundamentally under the control of females, providing avenues for females to evolve multiple mating as a defence against hybridization, with the counterintuitive outcome that promiscuity reinforces isolation and may promote speciation.

Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program STRUCTURE.

Reproducibility is the benchmark for results and conclusions drawn from scientific studies, but systematic studies on the reproducibility of scientific results are surprisingly rare. Moreover, many modern statistical methods make use of 'random walk' model fitting procedures, and these are inherently stochastic in their output. Does the combination of these statistical procedures and current standards of data archiving and method reporting permit the reproduction of the authors' results? To test this, we reanalysed data sets gathered from papers using the software package STRUCTURE to identify genetically similar clusters of individuals. We find that reproducing structure results can be difficult despite the straightforward requirements of the program. Our results indicate that 30% of analyses were unable to reproduce the same number of population clusters. To improve this, we make recommendations for future use of the software and for reporting STRUCTURE analyses and results in published works.

Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation.

1. Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2. We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3. Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4. We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.

Male and female Anolis carolinensis maintain their dimorphism despite the presence of novel interspecific competition.

Natural selection favors sexual dimorphism that reduces resource competition between the sexes of the same species. However, niche partitioning among interspecific competitors should counter such divergence, as partitioning the niche results in smaller total niche widths for each individual species, leaving less room for the sexes to diverge. A straightforward (and long-standing) hypothesis emerges: species in competitor-rich ecological communities should show less sexual dimorphism than species in competitor-poor ecological communities. Here, we test this prediction using a well-documented natural experiment generated by the recent arrival of Anolis sagrei to a set of small islands in Mosquito Lagoon, Florida, containing Anolis carolinensis. Despite known interspecific habitat partitioning and rapid evolution in habitat-use traits by A. carolinensis in this system, sexual dimorphism between male and female A. carolinensis was not reduced as predicted on two-species islands relative to islands with only A. carolinensis. This is consistent with a small but growing body of empirical tests of the dimorphism-richness hypothesis that have been ambiguous in their support at best. A rethinking of the validity of this intuitive hypothesis is needed.

Temporal differences in food abundance promote coexistence between two congeneric passerines.

Many related species share the same environment and utilize similar resources. This is surprising because based on the principle of competitive exclusion one would predict that the superior competitor would drive the other species to extinction; coexistence is only predicted if interspecific competition is weaker than intraspecific competition. Interspecific competition is frequently reduced by differential resource use, resulting in habitat segregation. In this paper, we use the closely related collared and pied flycatcher to assess the potential of habitat differences to affect interspecific competition through a different mechanism, namely by generating temporal differences in availability of similar food resources between the two species. We found that the tree species composition of the breeding territories of the two species differed, mainly by a higher abundance of coniferous species around nest-boxes occupied by pied flycatchers. The temporal availability of caterpillars was measured using frass traps under four deciduous and two coniferous tree species. Deciduous tree species showed an early and narrow peak in abundance, which contrasted with the steady increase in caterpillar abundance in the coniferous tree species through the season. We subsequently calculated the predicted total caterpillar biomass available in each flycatcher territory. This differed between the species, with biomass decreasing more slowly in pied flycatcher territories. Caterpillar biomass is strongly correlated with the reproductive success of collared flycatchers, but much less so with pied flycatchers. However, caterpillar availability can only partly explain the differences in seasonal decline of reproductive success between the two species; we discuss additional factors that may contribute to this species difference. Overall, our results are consistent with the suggestion that minor habitat differences between these two species may contribute to promoting their coexistence.

Natural and sexual selection against hybrid flycatchers.

While sexual selection is generally assumed to quickly cause or strengthen prezygotic barriers between sister species, its role in causing postzygotic isolation, through the unattractiveness of intermediate hybrids, is less often examined. Combining 24 years of pedigree data and recently developed species-specific molecular markers from collared (Ficedula albicollis) and pied (Ficedula hypoleuca) flycatchers and their hybrids, we were able to quantify all key components of fitness. To disentangle the relative role of natural and sexual selection acting on F1 hybrid flycatchers, we estimated various fitness components, which when combined represent the total lifetime reproductive success of F1 hybrids, and then compared the different fitness components of F1 hybrids to that of collared flycatchers. Female hybrid flycatchers are sterile, with natural selection being the selective force involved, but male hybrids mainly experienced a reduction in fitness through sexual selection (decreased pairing success and increased rate of being cuckolded). To disentangle the role of sexual selection against male hybrids from a possible effect of genetic incompatibility (on the rate of being cuckolded), we compared male hybrids with pure-bred males expressing intermediate plumage characters. Given that sexual selection against male hybrids is a result of their intermediate plumage, we expect these two groups of males to have a similar fitness reduction. Alternatively, hybrids have reduced fitness owing to genetic incompatibility, in which case their fitness should be lower than that of the intermediate pure-bred males. We conclude that sexual selection against male hybrids accounts for approximately 75% of the reduction in their fitness. We discuss how natural and sexual selection against hybrids may have different implications for speciation and conclude that reinforcement of reproductive barriers may be more likely when there is sexual selection against hybrids.

Opsin expression predicts male nuptial color in threespine stickleback.

Theoretical models of sexual selection suggest that male courtship signals can evolve through the build-up of genetic correlations between the male signal and female preference. When preference is mediated via increased sensitivity of the signal characteristics, correlations between male signal and perception/sensitivity are expected. When signal expression is limited to males, we would expect to find signal-sensitivity correlations in males. Here, we document such a correlation within a breeding population of threespine stickleback mediated by differences in opsin expression. Males with redder nuptial coloration express more long-wavelength-sensitive (LWS) opsin, making them more sensitive to orange and red. This correlation is not an artifact of shared tuning to the optical microhabitat. Such correlations are an essential feature of many models of sexual selection, and our results highlight the potential importance of opsin expression variation as a substrate for signal-preference evolution. Finally, these results suggest a potential sensory mechanism that could drive negative frequency-dependent selection via male-male competition and thus maintain variation in male nuptial color.

Does migration of hybrids contribute to post-zygotic isolation in flycatchers?

In the face of hybridization, species integrity can only be maintained through post-zygotic isolating barriers (PIBs). PIBs need not only be intrinsic (i.e. hybrid inviability and sterility caused by developmental incompatibilities), but also can be extrinsic due to the hybrid's intermediate phenotype falling between the parental niches. For example, in migratory species, hybrid fitness might be reduced as a result of intermediate migration pathways and reaching suboptimal wintering grounds. Here, we test this idea by comparing the juvenile to adult survival probabilities as well as the wintering grounds of pied flycatchers (Ficedula hypoleuca), collared flycatchers (Ficedula albicollis) and their hybrids using stable isotope ratios of carbon (delta13C) and nitrogen (delta15N) in feathers developed at the wintering site. Our result supports earlier observations of largely segregated wintering grounds of the two parental species. The isotope signature of hybrids clustered with that of pied flycatchers. We argue that this pattern can explain the high annual survival of hybrid flycatchers. Hence, dominant expression of the traits of one of the parental species in hybrids may substantially reduce the ecological costs of hybridization.

Many-to-one form-to-function mapping weakens parallel morphological evolution.

Evolutionary ecologists aim to explain and predict evolutionary change under different selective regimes. Theory suggests that such evolutionary prediction should be more difficult for biomechanical systems in which different trait combinations generate the same functional output: "many-to-one mapping." Many-to-one mapping of phenotype to function enables multiple morphological solutions to meet the same adaptive challenges. Therefore, many-to-one mapping should undermine parallel morphological evolution, and hence evolutionary predictability, even when selection pressures are shared among populations. Studying 16 replicate pairs of lake- and stream-adapted threespine stickleback (Gasterosteus aculeatus), we quantified three parts of the teleost feeding apparatus and used biomechanical models to calculate their expected functional outputs. The three feeding structures differed in their form-to-function relationship from one-to-one (lower jaw lever ratio) to increasingly many-to-one (buccal suction index, opercular 4-bar linkage). We tested for (1) weaker linear correlations between phenotype and calculated function, and (2) less parallel evolution across lake-stream pairs, in the many-to-one systems relative to the one-to-one system. We confirm both predictions, thus supporting the theoretical expectation that increasing many-to-one mapping undermines parallel evolution. Therefore, sole consideration of morphological variation within and among populations might not serve as a proxy for functional variation when multiple adaptive trait combinations exist.

Contrasting effects of environment and genetics generate a continuum of parallel evolution.

Parallel evolution of similar traits by independent populations in similar environments is considered strong evidence for adaptation by natural selection. Often, however, replicate populations in similar environments do not all evolve in the same way, thus deviating from any single, predominant outcome of evolution. This variation might arise from non-adaptive, population-specific effects of genetic drift, gene flow or limited genetic variation. Alternatively, these deviations from parallel evolution might also reflect predictable adaptation to cryptic environmental heterogeneity within discrete habitat categories. Here, we show that deviations from parallel evolution are the consequence of environmental variation within habitats combined with variation in gene flow. Threespine stickleback (Gasterosteus aculeatus) in adjoining lake and stream habitats (a lake-stream 'pair') diverge phenotypically, yet the direction and magnitude of this divergence is not always fully parallel among 16 replicate pairs. We found that the multivariate direction of lake-stream morphological divergence was less parallel between pairs whose environmental differences were less parallel. Thus, environmental heterogeneity among lake-stream pairs contributes to deviations from parallel evolution. Additionally, likely genomic targets of selection were more parallel between environmentally more similar pairs. In contrast, variation in the magnitude of lake-stream divergence (independent of direction) was better explained by differences in lake-stream gene flow; pairs with greater lake-stream gene flow were less morphologically diverged. Thus, both adaptive and non-adaptive processes work concurrently to generate a continuum of parallel evolution across lake-stream stickleback population pairs.

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.

Identifying the African wintering grounds of hybrid flycatchers using a multi-isotope (δ2H, δ13C, δ15N) assignment approach.

Migratory routes and wintering grounds can have important fitness consequences, which can lead to divergent selection on populations or taxa differing in their migratory itinerary. Collared (Ficedula albicollis) and pied (F. hypoleuca) flycatchers breeding in Europe and wintering in different sub-Saharan regions have distinct migratory routes on the eastern and western sides of the Sahara desert, respectively. In an earlier paper, we showed that hybrids of the two species did not incur reduced winter survival, which would be expected if their migration strategy had been a mix of the parent species' strategies potentially resulting in an intermediate route crossing the Sahara desert to different wintering grounds. Previously, we compared isotope ratios and found no significant difference in stable-nitrogen isotope ratios (δ15N) in winter-grown feathers between the parental species and hybrids, but stable-carbon isotope ratios (δ13C) in hybrids significantly clustered only with those of pied flycatchers. We followed up on these findings and additionally analyzed the same feathers for stable-hydrogen isotope ratios (δ2H) and conducted spatially explicit multi-isotope assignment analyses. The assignment results overlapped with presumed wintering ranges of the two species, highlighting the efficacy of the method. In contrast to earlier findings, hybrids clustered with both parental species, though most strongly with pied flycatcher.

Premating reproductive barriers between hybridising cricket species differing in their degree of polyandry.

Understanding speciation hinges on understanding how reproductive barriers arise between incompletely isolated populations. Despite their crucial role in speciation, prezygotic barriers are relatively poorly understood and hard to predict. We use two closely related cricket species, Gryllus bimaculatus and G. campestris, to experimentally investigate premating barriers during three sequential mate choice steps. Furthermore, we experimentally show a significant difference in polyandry levels between the two species and subsequently test the hypothesis that females of the more polyandrous species, G. bimaculatus, will be less discriminating against heterospecific males and hence hybridise more readily. During close-range mating behaviour experiments, males showed relatively weak species discrimination but females discriminated very strongly. In line with our predictions, this discrimination is asymmetric, with the more polyandrous G. bimaculatus mating heterospecifically and G. campestris females never mating heterospecifically. Our study shows clear differences in the strength of reproductive isolation during the mate choice process depending on sex and species, which may have important consequences for the evolution of reproductive barriers.