Jennifer L. Gow

Speciation in reverse: morphological and genetic evidence of the collapse of a three‐spined stickleback (Gasterosteus aculeatus) species pair

Historically, six small lakes in southwestern British Columbia each contained a sympatric species pair of three‐spined sticklebacks (Gasterosteus aculeatus). These pairs consisted of a ‘benthic’ and ‘limnetic’ species that had arisen postglacially and, in four of the lakes, independently. Sympatric sticklebacks are considered biological species because they are morphologically, ecologically and genetically distinct and because they are strongly reproductively isolated from one another. The restricted range of the species pairs places them at risk of extinction, and one of the pairs has gone extinct after the introduction of an exotic catfish. In another lake, Enos Lake, southeastern Vancouver Island, an earlier report suggested that its species pair is at risk from elevated levels of hybridization. We conducted a detailed morphological analysis, as well as genetic analysis of variation at five microsatellite loci for samples spanning a time frame of 1977 to 2002 to test the hypothesis that the pair in Enos Lake is collapsing into a hybrid swarm. Our morphological analysis showed a clear breakdown between benthics and limnetics. Bayesian model‐based clustering indicated that two morphological clusters were evident in 1977 and 1988, which were replaced by 1997 by a single highly variable cluster. The most recent 2000 and 2002 samples confirm the breakdown. Microsatellite analysis corroborated the morphological results. Bayesian analyses of population structure in a sample collected in 1994 indicated two genetically distinct populations in Enos Lake, but only a single genetic population was evident in 1997, 2000, and 2002. In addition, genetic analyses of samples collected in 1997, 2000, and 2002 showed strong signals of ‘hybrids’; they were genetically intermediate to parental genotypes. Our results support the idea that the Enos Lake species pair is collapsing into a hybrid swarm. Although the precise mechanism(s) responsible for elevated hybridization in the lake is unknown, the demise of the Enos Lake species pair follows the appearance of an exotic crayfish, Pascifasticus lenisculus, in the early 1990s.

Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species.

Three‐spined sticklebacks (Gasterosteus aculeatus) are a powerful evolutionary model system due to the rapid and repeated phenotypic divergence of freshwater forms from a marine ancestor throughout the Northern Hemisphere. Many of these recently derived populations are found in overlapping habitats, yet are reproductively isolated from each other. This scenario provides excellent opportunities to investigate the mechanisms driving speciation in natural populations. Genetically distinguishing between such recently derived species, however, can create difficulties in exploring the ecological and genetic factors defining species boundaries, an essential component to our understanding of speciation. We overcame these limitations and increased the power of analyses by selecting highly discriminatory markers from the battery of genetic markers now available. Using species diagnostic molecular profiles, we quantified levels of hybridization and introgression within three sympatric species pairs of three‐spined stickleback. Sticklebacks within Priest and Paxton lakes exhibit a low level of natural hybridization and provide support for the role of reinforcement in maintaining distinct species in sympatry. In contrast, our study provides further evidence for a continued breakdown of the Enos Lake species pair into a hybrid swarm, with biased introgression of the ‘limnetic’ species into that of the ‘benthic’; a situation that highlights the delicate balance between persistence and breakdown of reproductive barriers between young species. A similar strategy utilizing the stickleback microsatellite resource can also be applied to answer an array of biological questions in other species’ pair systems in this geographically widespread and phenotypically diverse model organism.

Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks

Experimental work has provided evidence for extrinsic post‐zygotic isolation, a phenomenon unique to ecological speciation. The role that ecological components to reduced hybrid fitness play in promoting speciation and maintaining species integrity in the wild, however, is not as well understood. We addressed this problem by testing for selection against naturally occurring hybrids in two sympatric species pairs of benthic and limnetic threespine sticklebacks (Gasterosteus aculeatus). If post‐zygotic isolation is a significant reproductive barrier, the relative frequency of hybrids within a population should decline significantly across the life‐cycle. Such a trend in a natural population would give independent support to experimental evidence for extrinsic, rather than intrinsic, post‐zygotic isolation in this system. Indeed, tracing mean individual hybridity (genetic intermediateness) across three life‐history stages spanning four generations revealed just such a decline. This provides compelling evidence that extrinsic selection plays an important role in maintaining species divergence and supports a role for ecological speciation in sticklebacks.

QUANTIFYING THE CONSTRAINING INFLUENCE OF GENE FLOW ON ADAPTIVE DIVERGENCE IN THE LAKE-STREAM THREESPINE STICKLEBACK SYSTEM

Abstract The constraining effect of gene flow on adaptive divergence is often inferred but rarely quantified. We illustrate ways of doing so using stream populations of threespine stickleback (Gasterosteus aculeatus) that experience different levels of gene flow from a parapatric lake population. In the Misty Lake watershed (British Columbia, Canada), the inlet stream population is morphologically divergent from the lake population, and presumably experiences little gene flow from the lake. The outlet stream population, however, shows an intermediate phenotype and may experience more gene flow from the lake. We first used microsatellite data to demonstrate that gene flow from the lake is low into the inlet but high into the outlet, and that gene flow from the lake remains relatively constant with distance along the outlet. We next combined gene flow data with morphological and habitat data to quantify the effect of gene flow on morphological divergence. In one approach, we assumed that inlet stickleback manifest well-adapted phenotypic trait values not constrained by gene flow. We then calculated the deviation between the observed and expected phenotypes for a given habitat in the outlet. In a second approach, we parameterized a quantitative genetic model of adaptive divergence. Both approaches suggest a large impact of gene flow, constraining adaptation by 80–86% in the outlet (i.e., only 14–20% of the expected morphological divergence in the absence of gene flow was observed). Such approaches may be useful in other taxa to estimate how important gene flow is in constraining adaptive divergence in nature.

Little impact of hatchery supplementation that uses native broodstock on the genetic structure and diversity of steelhead trout revealed by a large-scale spatio-temporal microsatellite survey

Artificial breeding programs initiated to enhance the size of animal populations are often motivated by the desire to increase harvest opportunities. The introduction of non‐native genotypes, however, can have negative evolutionary impacts. These may be direct, such as introgressive hybridization, or indirect via competition. Less is known about the effects of stocking with native genotypes. We assayed variation at nine microsatellite loci in 902 steelhead trout (Oncorhynchus mykiss) from five rivers in British Columbia, Canada. These samples were collected over 58 years, a time period that spanned the initiation of native steelhead trout broodstock hatchery supplementation in these rivers. We detected no changes in estimates of effective population size, genetic variation or temporal genetic structure within any population, nor of altered genetic structure among them. Genetic interactions with nonmigratory O. mykiss, the use of substantial numbers of primarily native broodstock with an approximate 1:1 male‐to‐female ratio, and/or poor survival and reproductive success of hatchery fish may have minimized potential genetic changes. Although no genetic changes were detected, ecological effects of hatchery programs still may influence wild population productivity and abundance. Their effects await the design and implementation of a more comprehensive evaluation program.

A test of hybrid growth disadvantage in wild, free-ranging species pairs of threespine stickleback (Gasterosteus aculeatus) and its implications for ecological speciation.

Ecological speciation is the evolution of reproductive isolation as a direct or indirect consequence of divergent natural selection. Reduced performance of hybrids in nature is thought to be an important process by which natural selection can favor the evolution of assortative mating and drive speciation. Benthic and limnetic sympatric species of threespine stickleback (Gasterosteus aculeatus) are adapted to alternative trophic niches (bottom browsing vs. open water planktivory, respectively) and reduced feeding performance of hybrids is thought to have contributed to the evolution of reproductive isolation. We tested this “hybrid‐disadvantage hypothesis” by inferring growth rates from otoliths sampled from wild, free‐ranging benthic, limnetic, and hybrid sticklebacks in two lakes. There were significant differences in growth rate between lakes, life‐history stages, and among years (maximum P = 0.02), as well as interactions between most factors, but not between hybrid and parental species sticklebacks in most comparisons. Our results provide little evidence of a growth disadvantage in hybrid sticklebacks when free‐ranging in nature. Although trophic ecology per se may contribute less to ecological speciation than envisioned, it may act in concert with other aspects of stickleback biology, such as interactions with parasites, predators, competitors, and/or sexual selection, to present strong multifarious selection against hybrids.

Photoplethysmogram Processing Using an Adaptive Single Frequency Phase Vocoder Algorithm

We have previously designed a pulse oximeter connected to a mobile phone, called the Phone Oximeter, for clinical decision making based on photoplethysmography. The limited battery and computational resources demand efficient and low-power algorithms for the Phone Oximeter to be effective in resource-poor and remote areas. We present two new algorithms for the fast and economical estimation of heart rate (HR) from the photoplethysmogram (PPG). One method estimates the HR frequency by adaptively modeling the PPG wave with a sine function using a modified phase vocoder. The other method uses the obtained wave as an envelope for the detection of peaks in the PPG signal. HR is computed using the vocoder center frequency or the peak intervals in a histogram, respectively. PPG data obtained from 42 subjects were processed with the vocoder algorithms and, for comparison, with two traditional methods that use filtering algorithms (Pan-Tompkins) and frequency domain transformations (Fast-Fourier Transform). We compared HR estimates obtained from these four methods to the reference HR obtained from a electrocardiogram. The two vocoder methods performed at least as well as the two traditional methods in terms of normalized root mean sqare error and robustness towards artifacts. Experiments on a mobile device prototype showed comparable speed performance of the vocoder algorithms with the Pan-Tompkins algorithm while the frequency domain approach was nearly two orders of magnitude slower. These results point to further developments using a combination of both vocoder HR estimation methods that will enable the robust implementation of adaptive phase vocoders into mobile device health applications.

The mating game: do opposites really attract?

When selecting a mate, females of many species face a complicated decision: choosing a very closely related mate will lead to inbreeding, while choosing a mate who is too genetically dissimilar risks breaking up beneficial gene complexes or local genetic adaptations. To ensure the best genetic quality of their offspring, the perfect compromise lies somewhere in between: an optimally genetically dissimilar partner. Empirical evidence demonstrating female preference for genetically dissimilar mates is proof of the adage ‘opposites attract’. In stark contrast, Chandler & Zamudio (2008) show in this issue of Molecular Ecology that female spotted salamanders often choose males that are genetically more similar to themselves (although not if the males are small). Along with other recent work, these field studies highlight the broad spectrum of options available to females with respect to relatedness in their choice of mate that belies this rule of thumb.