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Plant J 40 : — Allopatry may start the process off, but the evolution of internal i. If internal barriers to gene flow do not evolve, individuals from the two parts of the population will freely interbreed if they come back into contact.
Whatever genetic differences may have evolved will disappear as their genes mix back together. Speciation requires that the two incipient species be unable to produce viable offspring together or that they avoid mating with members of the other group.
Here are some of the barriers to gene flow that may contribute to speciation. They result from natural selection, sexual selection, or even genetic drift:. Different species of bowerbird construct elaborate bowers and decorate them with different colors in order to woo females. Evolutionary changes in mating rituals, such as bower construction, can contribute to speciation.
Satin bowerbird photo courtesy of Graeme Guy. These damselfly penises illustrate just how complex insect genitalia may be. Image adapted from Eberhard, W. Some ephippia from intrapopulation crosses in D. Overall, this RIB barrier was symmetrical between sympatric and allopatric populations. The unexpectedly high level of RI F1hatching could be a result of genetic incompatibilities between the two species as well as among distant populations.
However, as we induced hatching using the same set of cues across all crosses, it is possible that some of the failures to hatch could be due to the wrong cue. Out of the individuals that hatched from ephippia, individuals survived to adulthood and produced a first brood Similar proportions of F1 survivorship were found for allopatric and sympatric heterospecific crosses Fig.
F1 survivorship RIB estimates were similar in D. We calculated habitat and temporal isolation between D.
Based on ten population genetic datasets Additional file 1 : Table S3 , we determined mean habitat isolation between D. We acknowledge that habitat isolation estimate could be inflated due to the limited ldha data readily available and our decision to exclude the SF genotypes known to be obligately asexual in nature in the calculation. Ecological barriers habitat and temporal isolation have had the greatest contribution to reproductive isolation compared to all nonecological prezygotic and postzygotic barriers Table 2.
We find that ecological prezygotic RIB contributes to The prezygotic and postzygotic non-ecological barriers are much weaker contributing to only 0. Of the reproductive isolating barriers examined, none had the means to restrict gene flow between D. When comparing non-ecological isolating barriers, the greatest contribution to reproductive isolation was provided by F1 hatching success followed by F1 zygotic mortality and F1 survivorship.
While contemporary levels of gene flow estimated based on nuclear markers are relatively low between Daphnia pulex and Daphnia pulicaria [ 42 , 59 ], likely due to strong ecological barriers, these species hybridize readily under laboratory conditions. We find that ecological barriers habitat and temporal isolation produced the largest contribution towards restricting gene flow.
None of the non-ecological RIBs that we examined in this study prezygotic or postzygotic had the capability of completely restricting gene flow between D. We found asymmetry in the non-ecological prezygotic isolating barrier, where D. Interestingly, we found enhanced intrinsic postzygotic isolating barriers between geographically far populations of D. When examining prezygotic isolating barriers between D. As the two species inhabit distinct habitats and exhibit different life history traits as a result of such habitat differences, shifts in their timing of sexual reproduction could have evolved as a by-product of these differences.
The induction of sexual reproduction depends mainly on photoperiod but also on food level or population density [ 61 , 62 , 63 ]. Ecological prezygotic isolating barriers have been previously hypothesized to be a major contributor in restricting gene flow between the two species [ 41 , 59 ], and this observation is consistent with studies on other ecological species suggesting the importance of ecological divergence in promoting speciation [ 29 , 64 ]. In the absence of ecological prezygotic barriers, D.
While our study did not distinguish between behavioural and mechanical isolation in these two species, previous studies point to the importance of these reproductive barriers in cladocerans [ 65 , 66 , 67 ], and observations in mating behaviour in D.
Previous studies reported successful laboratory crosses between D. Although we conducted successful crosses in both directions, comparisons between the reciprocal crosses indicate significantly lower mating-fertilization success in D. The efficiency of prezygotic reproductive barriers in restricting gene flow depends on the level and symmetry of historical gene flow between the sister species. Gene flow can be symmetrical or asymmetrical and this can influence the degree of symmetry in reproductive barriers.
For example, flooding events from lakes to ponds often result in D. In nature, the maternal parent of most hybrids is D. In this scenario, the probability of D.
Unidirectional hybridization between closely related daphniid species appears to be common [ 71 ], as an example, experimental crosses of Daphnia galeata and Daphnia cucullata exhibited asymmetrical reproductive isolating barriers [ 72 ].
Furthermore, the addition of multiple reproductive barriers is necessary for complete isolation [ 17 , 18 ]. Intrinsic postzygotic isolating barriers in association with a reduction in hybrid viability or fitness can be due to genetic incompatibilities such as Bateson-Dobzhansky-Muller BDM incompatibilities between the genomes of two species. According to the BDM model, incipient species that diverge in allopatry accumulate different mutational backgrounds, and during secondary contact, hybrids show a reduction in fitness compared to parental species due to negative epistatic interactions between the two genomes [ 73 , 74 , 75 ].
Hybrid performance can be further reduced in subsequent generations due to recombination events that break up epistatic interactions, facilitating reproductive isolation between the parental species.
In the absence of prezygotic isolating barriers, intrinsic postzygotic isolation appears to play a substantial role in restricting gene flow between D. Of the three intrinsic postzygotic barriers that we examined, F1 hatching had the greatest influence in restricting gene flow.
In contrast, F1 survivorship was consistently high Fig. Overall, postzygotic isolating barriers displayed symmetry in their ability to restrict gene flow between D.
While postzygotic isolating barriers were thought to evolve slower in comparison to prezygotic isolating barriers [ 13 ], it appears that postzygotic isolation is important in restricting gene flow between these two species, which have diverged relatively recently e. Consistent with our results, [ 72 ] found low hatching and survivorship in experimental crosses between two closely related Daphnia species, Daphnia cucullata and Daphnia galeata. Similarly, intrinsic postzygotic isolating barriers play an important role for species that are currently in the process of ecological speciation [ 76 ].
One of our most unexpected findings was the very low hatching and survivorship experienced by conspecific populations of D. This could be due to genetic incompatibilities in F1 hybrids during hatching and development, impeding survival to adulthood.
Previous population genetics studies reveal an unexpectedly high level of genetic subdivision within D. Furthermore, theory suggests that fixation and accumulation of genetic incompatibilities occurs quickly in the absence of gene flow [ 78 ]. RIB studies of incipient species have also found the importance of intrinsic postzygotic isolation for diverging populations [ 34 , 76 , 79 ].
As hatching requirements vary between as well as within species [ 87 , 88 ], and depend on environmental cues, it is possible that our experimental protocol was unable to reproduce the appropriate cues for hatching D. The timing of storage of ephippia in the dark was variable in our study from 1 month to about 1. This variation in storage time was accounted for in our generalized linear models and was found to have a negligible effect on hatching success Additional file 2 : Figure S2.
The process of speciation is shaped by the evolutionary forces responsible for building and maintaining prezygotic and postzygotic reproductive barriers. The attention is often placed on how RIB emerge and a lot less is known about how barriers are maintained but see [ 89 ]. Reinforcement of prezygotic barriers is thought to be a major evolutionary force for strengthening such barriers.
In reinforcement, mating discrimination and mating preferences are enhanced in sympatric populations, where hybridization is most likely to occur, compared to allopatric populations [ 90 , 91 , 92 ].
Signatures of reinforcement have been found in a wide variety of taxa such as insects [ 93 , 94 ], fish [ 95 ], birds [ 96 ] and mammals [ 97 ]. However, we found no evidence for stronger prezygotic isolation in sympatry than in allopatry. Instead, we found evidence of asymmetrical reproductive isolating barriers for non-ecological prezygotic isolating barrier.
Asymmetrical reproductive barriers have been found in a variety of organisms, and this pattern can occur in prezygotic [ 98 , 99 ], postzygotic [ , , ], or both types of barriers [ 10 , 17 , ]. Additionally, we find evidence that postzygotic isolating mechanisms play an important role in restricting gene flow between intraspecific lineages of D.
This finding consolidated early speciation studies which found support for postzygotic isolating barriers among intraspecific lineages of the rainwater killifish Lucania parva Cyprinodontiformes: Fundulidae [ 24 ] and the spring peeper chorus frog Pseudacris crucifer Anura: Hylidae [ 34 ]. Other incipient plant species across various stages of the speciation continuum show the importance of postzygotic isolating barriers rather than prezygotic isolating barriers in restricting gene flow [ 22 , , ].
Collectively, these studies suggest that genetic incompatibilities accumulating between diverging populations could often mark the initial stages of speciation [ ]. This study examines prezygotic and postzygotic reproductive isolating barriers across the speciation continuum: from conspecific populations that are at the early stages of divergence to closely related species, within the young species complex of Daphnia pulex.
We examine barriers that are emerging the initial stage of speciation , as well as the barriers that are accumulating latter in the speciation process. We find that postzygotic isolating barriers appear to be responsible for the genetic subdivision reported within the Daphnia pulex lineage, suggestive of incipient speciation.
We also find that ecological barriers are currently very strong and have the largest contribution towards restricting gene flow among the well-recognized ecological species. Thus, our results indicate that while non-ecological postzygotic isolating barriers were likely important during the initial stages of speciation, ecological, prezygotic isolating barriers are currently responsible for maintaining species boundaries.
Our findings have implications for our understanding of the process of speciation revealing that current acting barriers are often not the same as early acting barriers and that the role of postzygotic isolation is likely underestimated, particularly when considering the very early stages of speciation.
To quantify non-ecological RIB, we established Daphnia clonal lineages from 13 populations 7 ponds and 6 lakes; Table 1 , Additional file 2 : Figure S1. All isolates were identified by morphology [ 47 ] and molecular markers using the protocol described by [ 59 ]. The lactate dehydrogenase A locus ldh A was amplified to differentiate the pond species D. To confirm reproduction by cyclical parthenogenesis sexual production of diapausing eggs , females were maintained in the absence of males and the deposition or lack thereof of dormant embryos in the ephippia were recorded based on the protocol from [ ] Table 1.
Mature females carrying ephippia were selected from cultures. Males were isolated from cultures for at least 3 days prior to setting up the cross to ensure sexual maturity see Additional file 1. From the established clonal lines, no-choice crosses were set up to examine the absolute and relative contributions of non-ecological reproductive isolating barriers acting between D.
We conducted conspecific crosses for D. All crosses were replicated at least three times using individuals of the same genotype. We used identical female and male genotypes for the focal cross and the corresponding reverse cross. For each of the cross categories, we constructed at least two different crosses, using female and male genotypes originating from different habitats e. Therefore, each cross category included individuals from a minimum of four habitats.
As species of the D. To estimate RIB among populations conspecific crosses , as well as between species heterospecific crosses , intrapopulation crosses were constructed as a baseline of performance considered as C in our calculation for RIB , where individuals of distinct genotypes originating from the same habitat were crossed e.
We define allopatric populations as populations of Daphnia with low or restricted level of gene flow between lakes and ponds. We sampled D. Therefore, current gene flow between the two species is considered negligible. Sympatric populations were sampled from regions where we expect a high probability of gene flow between lakes and ponds e. Each cross was assessed for the production of dormant embryos, which is a reflection of successful mating and fertilization.
Females can revert back to parthenogenesis at any time during the experiment. Thus, the first time the female produced an amictic brood, the brood was removed and the cross was allowed to continue with the expectation that the female would revert back to the sexual phase.
However, on the second amictic clutch, the cross was terminated. Each cross was maintained until a maximum of five ephippia were collected. Ephippia were opened under a Leica dissecting microscope. Each ephippium could have either 0, 1, or 2 dormant embryos. For each cross, the first ephippium produced by the female was opened and scored for dormant embryos, but not included in the calculation due to the possibility of previous fertilization prior to cross set up.
Morphological analyses of daphniid females found no evidence of sperm storage receptacles [ , ], and therefore we expect that females do not store sperm. All subsequent ephippia produced were included in the calculation. We examined three intrinsic postzygotic isolating barriers: F1 zygotic mortality, F1 hatching success, and F1 survivorship. For F1 zygotic mortality, we opened all ephippia at the end of the hatching assay to examine the appearance and quality of the dormant embryos.
A score of 0 was assigned to embryos that began the process of development without successfully hatching, and a score of 1 was given to embryos that remained dormant and did not hatch. If fungal infections were observed, the embryos were categorized as inviable and given a score of 0.
If dormant embryos successfully hatched, they were not included in the F1 zygotic mortality dataset. F1 zygotic mortality was calculated as the number of viable embryos over the total number of dormant embryos. We set up the hatching assay during spring to promote favourable hatching conditions. We used natural spring water for rehydration to mimic natural freshwater habitats. Hatching ephippia in laboratory conditions is not without its caveats, as hatching is largely dependent on environmental cues [ 87 , , ].
Thus, embryos may not hatch because they did not detect the appropriate cues rather than having developmental defects. However, by exposing all cross categories to the same hatching cue, we standardize the performance of each cross category against the performance of the intrapopulation crosses.
F1 hatching success was assessed by the number of dormant embryos that have hatched over the total number of dormant embryos that were recorded from the mating success dataset. Survivorship was scored on a scale of 0 to 1 by assessing whether an individual was not able to reach adulthood 0 or reached adulthood and produced their first brood of clonal daughters 1.
F1 survivorship was calculated as the number of individuals that survived over the total number of hatched embryos. To estimate habitat isolation RI Habitat between D. We calculated the number of instances of encountering both species in a particular habitat by recording whether homozygote SS D. We opted to omit heterozygote SF genotypes from the dataset, as SF genotypes found in nature are obligate parthenogenetic and not true F1 hybrids see [ , ].
We calculated habitat isolation for each study as follows:. This RI metric ranges from 0 no restriction of gene flow to 1 complete restriction of gene flow. We ran 10, bootstrap iterations to calculate the confidence intervals Fig.
As facultative parthenogens, daphniids reproduce sexually during a few weeks of the year, although the exact timing of reproduction can vary among populations [ 77 ]. To estimate temporal isolation RI Temporal between the two species, we use temporal datasets from [ 50 , 60 ], which report percent occurrence of sexually reproducing individuals of D.
We calculated temporal isolation between the two species as:. We took the mean of these two datasets as an estimate of temporal isolation between the two species Table 2. We calculated the strength of each reproductive isolating barrier RI i using methods modified from [ 20 ]:. Considering the extreme levels of subdivision that occur within these two species [ 40 , 77 ], and the uncertainty of whether the species exhibit genetic cohesion or are undergoing cryptic speciation, we define C as the mean frequency of successes of intrapopulation crosses in both D.
Therefore, the RI metric ranges from 0 to 1, where 1 is the complete restriction of gene flow, and 0 indicates that there is no restriction of gene flow. We calculated the RI i of each independent cross before taking the mean for each cross category to determine RIB. All our statistical analyses were done using R version 3.
We implemented generalized linear mixed effects models glmm to account for random effects e. For each of our reproductive isolating barriers, we tested each response variable against the different cross categories as our dependent variables e. A post-hoc Tukey test multcomp [ ] was implemented for multiple comparisons between the different cross categories. In our mating-fertilization dataset, we constructed a poisson glmm with a log link function, where our response variable is the number of dormant embryos observed and our fixed variable is the cross category.
We compared nested and non-nested models between the different cross categories; however, both glmms had similar Akaike Information Criterion AIC values. To account for temporal pseudoreplication, the number of trials was incorporated as a random effect e.
Additionally, we accounted for differences in genotypes used in constructing each cross as a random effect. We compared nested and non-nested models of the different cross categories and found that non-nested models fitted better due to lower AIC values. We accounted for the differences in storage time by incorporating it into the model as a random effect.
We also considered differences in genotypes that were used to construct each cross as a random effect. For the F1 survivorship dataset, we constructed a binomial glmm with a logit link function, where the response variable is survivorship and the fixed variable is cross category.
We compared nested and non-nested models of the different cross categories and found that both models had similar fit to the dataset due to similar AIC values. We accounted for any differences in genotypes that were used to construct each cross as a random effect. We were interested in comparing RIB estimates between sympatric and allopatric crosses and examining the symmetry of these barriers respective of the directionality of the cross.
Total reproductive isolation between D. The absolute contribution AC n of each RIB was calculated as the multiplicative function of its independent strength RI i and the amount of gene flow that remains unrestricted from its previous barriers that are acting earlier:. Total reproductive isolation is then calculated based on the sum of the absolute strengths of each barrier based on calculations from [ 4 ].
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