Maternal influences on population dynamics: evidence from an exploited freshwater fish.

We used a field experiment, population modeling, and an analysis of 30 years of data from walleye (Sander vitreus; a freshwater fish) in Lake Erie to show that maternal influences on offspring survival can affect population dynamics. We first demonstrate experimentally that the survival of juvenile walleye increases with egg size (and, to a lesser degree, female energy reserves). Because egg size in this species tends to increase with maternal age, we then model these maternal influences on offspring survival as a function of maternal age to show that adult age structure can affect the maximum rate at which a population can produce new adults. Consistent with this hypothesis, we present empirical evidence that the maximum reproductive rate of an exploited population of walleye was approximately twice as high when older females were abundant as compared to when they were relatively scarce. Taken together, these results indicate that age- or size-based maternal influences on offspring survival can be an important mechanism driving population dynamics and that exploited populations could benefit from management strategies that protect, rather than target, reproductively valuable individuals.

Non-breeding season events influence sexual selection in a long-distance migratory bird.

The study of sexual selection has traditionally focused on events and behaviours immediately surrounding copulation. In this study, we examine whether carry-over effects from the non-breeding season can influence the process of sexual selection in a long-distance migratory bird, the American redstart (Setophaga ruticilla). Previous work on American redstarts demonstrated that overwintering in a high-quality habitat influences spring departure dates from the wintering grounds, advances arrival dates on the breeding grounds and increases apparent reproductive success. We show that the mixed-mating strategy of American redstarts compounds the benefits of overwintering in high-quality winter habitats. Males arriving to breed in Canada from high-quality winter habitats arrive earlier than males from poor-quality habitats, resulting in a lower probability of paternity loss, a higher probability of achieving polygyny and ultimately higher realized reproductive success. Such results suggest that the process of sexual selection may be influenced by events interacting throughout the annual cycle.

Ecological linkages between community and genetic diversity in zooplankton among boreal shield lakes.

Ecological linkages between species diversity in communities and genetic diversity in populations have potential to influence the assembly of communities in habitats recovering from human disturbance, but few studies have attempted to synthesize relationships between these levels of biological organization, especially for locally adapted species. No such studies have been done in freshwater ecosystems despite the plethora of environmental stressors plaguing aquatic communities around the world. We present the first study to test (1) whether diversity and dissimilarity among communities and populations of a locally adapted species are correlated and (2) whether communities and population haplotypes respond differently to environmental selection and spatial structure of habitats. We used a fragment of mitochondrial DNA (mtDNA) belonging to the gene cytochrome oxidase subunit I (COI) as a neutral tag to discriminate among different population haplotype variants. In boreal lakes with different histories of exposure to anthropogenic acidification, diversity and dissimilarity metrics for crustacean zooplankton communities and locally adapted populations of an abundant and broadly distributed calanoid copepod species, Leptodiaptomus minutus, did not correlate. This discord was likely because zooplankton communities responded more strongly to acidity and acidity-related environmental variables than spatial structure of lakes, whereas the distribution of L. minutus haplotypes was more strongly governed by spatial structure of lakes than environmental selection. Although spatial structure was the dominant driver of haplotype structure among L. minutus lake populations, there were similarities in the types of environmental variables that influenced the distributions of species in communities and haplotypes in populations. How haplotype diversity among populations relates to community diversity depends on the relative influence of spatial structure of habitats and selection at each of these scales of biological organization.

Multi-character perspectives on the evolution of intraspecific differentiation in a neotropical hylid frog.

BACKGROUND: Multi-character empirical studies are important contributions to our understanding of the process of speciation. The relatively conserved morphology of, and importance of the mate recognition system in anurans, combined with phylogenetic tools, provide an opportunity to address predictions about the relative role of each in the process of speciation. We examine the relationship among patterns of variation in morphology, call characters, and 16S gene sequences across seven populations of a neotropical hylid frog, Hyla leucophyllata, to infer their relative importance in predicting the early stages of population differentiation. RESULTS: Multivariate analyses demonstrate that both morphological and call characteristics were significantly variable among populations, characterized by significantly lower intra-population dispersion in call space than morphological space, and significantly greater among-population variation in call structure. We found lack of concordance between a 16S DNA phylogeny of Hyla leucophyllata and the significant population-level differentiation evident in both external morphology and male advertisement call. Comparisons of the reconstructed gene trees to simulated lineages support the notion that variation in call cannot be simply explained by population history. CONCLUSION: Discordance among traits may reflect sampling biases (e.g. single genetic marker effects), or imply a decoupling of evolution of different suites of characters. Diagnostic differences among populations in call structure possibly reflect local selection pressures presented by different heterospecific calling assemblages and may serve as a precursor of species-wide differentiation. Differentiation among populations in morphology may be due to ecophenotypic variation or to diversifying selection on body size directly, or on frequency attributes of calls (mediated by female choice) that show a strong relationship to body size.

The origin and diversification of Galapagos mockingbirds.

Evolutionary radiations of colonists on archipelagos provide valuable insight into mechanisms and modes of speciation. The apparent diversification of Galapagos mockingbirds (Nesomimus) provoked Darwin's initial conception of adaptive radiation, but the monophyly of this historically important exemplar has not been evaluated with molecular data. Additionally, as with most Galapagos organisms, we have a poor understanding of the temporal pattern of diversification of the mockingbirds following colonization(s) from source populations. Here we present a molecular phylogeny of Galapagos and other mockingbird populations based on mitochondrial sequence data. Monophyly of Galapagos mockingbirds was supported, suggesting a single colonization of the archipelago followed by diversification. Our analyses also indicate that Nesomimus is nested within the traditional genus Mimus, making the latter paraphyletic, and that the closest living relatives of Galapagos mockingbirds appear to be those currently found in North America, northern South America, and the Caribbean, rather than the geographically nearest species in continental Ecuador. Thus, propensity for over-water dispersal may have played a more important role than geographic proximity in the colonization of Galapagos by mockingbirds. Within Galapagos, four distinct mitochondrial DNA clades were identified. These four clades differ from current taxonomy in several important respects. In particular, mockingbirds in the eastern islands of the archipelago (Española, San Cristóbal, and Genovesa) have very similar mitochondrial DNA sequences, despite belonging to three different nominal species, and mockingbirds from Isabela, in the west of the archipelago, are more phylogenetically divergent than previously recognized. Consistent with current taxonomy is the phylogenetic distinctiveness of the Floreana mockingbird (N. trifasciatus) and close relationships among most mockingbirds from the central and northern region of the archipelago (currently considered conspecific populations of N. parvulus). Overall, phylogeographic patterns are consistent with a model of wind-based dispersal within Galapagos, with colonization of more northerly islands by birds from more southern populations, but not the reverse. Further radiation in Galapagos would require coexistence of multiple species on individual islands, but this may be prevented by relatively limited morphological divergence among mockingbirds and by lack of sufficient habitat diversity in the archipelago to support more than one omnivorous mimid.

Genetic connectivity across marginal habitats: the elephants of the Namib Desert.

Locally isolated populations in marginal habitats may be genetically distinctive and of heightened conservation concern. Elephants inhabiting the Namib Desert have been reported to show distinctive behavioral and phenotypic adaptations in that severely arid environment. The genetic distinctiveness of Namibian desert elephants relative to other African savanna elephant (Loxodonta africana) populations has not been established. To investigate the genetic structure of elephants in Namibia, we determined the mitochondrial (mt) DNA control region sequences and genotyped 17 microsatellite loci in desert elephants (n = 8) from the Hoanib River catchment and the Hoarusib River catchment. We compared these to the genotypes of elephants (n = 77) from other localities in Namibia. The mtDNA haplotype sequences and frequencies among desert elephants were similar to those of elephants in Etosha National Park, the Huab River catchment, the Ugab River catchment, and central Kunene, although the geographically distant Caprivi Strip had different mtDNA haplotypes. Likewise, analysis of the microsatellite genotypes of desert-dwelling elephants revealed that they were not genetically distinctive from Etosha elephants, and there was no evidence for isolation by distance across the Etosha region. These results, and a review of the historical record, suggest that a high learning capacity and long-distance migrations allowed Namibian elephants to regularly shift their ranges to survive in the face of high variability in climate and in hunting pressure.

Playback of colony sound alters the breeding schedule and clutch size in zebra finch (Taeniopygia guttata) colonies.

The hypothesis that social stimulation, derived from the presence and activities of conspecifics, can hasten and synchronize breeding in colonies of birds was tested. A modified playback/recorder system was used to continuously exaggerate the amount of colony sound available to zebra finches throughout their courtship period. Males that heard 'sound supplements' generated from their own colony sang more than males in control colonies that did not receive playback; males that heard samples from a different colony, sang at an intermediate level. Females that were exposed to the vocalizations of their mate and playback from a colony other than their own, laid eggs earlier and more synchronously than females in control colonies. Females that heard the vocalizations of their mate along with playback samples generated from their own colony, laid eggs more synchronously but not earlier than control females. Both acoustic treatments caused females to lay larger clutches. Social stimulation influences the breeding schedule and clutch size in zebra finch colonies. If there are advantages associated with these effects, social stimulation may contribute to the maintenance of colonial breeding systems.

Controlling for the effects of history and nonequilibrium conditions in gene flow estimates in northern bullfrog (Rana catesbeiana) populations.

Nonequilibrium conditions due to either allopatry followed by secondary contact or recent range expansion can confound measurements of gene flow among populations in previously glaciated regions. We determined the scale at which gene flow can be estimated among breeding aggregations of bullfrogs (Rana catesbeiana) at the northern limit of their range in Ontario, Canada, using seven highly polymorphic DNA microsatellite loci. We first identified breeding aggregations that likely share a common history, determined from the pattern of allelic richness, factorial correspondence analysis, and a previously published mtDNA phylogeography, and then tested for regional equilibrium by evaluating the association between pairwise F(ST) and geographic distance. Regional breeding aggregations in eastern Ontario separated by <100 km were determined to be at or near equilibrium. High levels of gene flow were measured using traditional F-statistics and likelihood estimates of Nm. Similarly high levels of recent migration (past one to three generations) were estimated among the breeding aggregations using nonequilibrium methods. We also show that, in many cases, breeding aggregations separated by up to tens of kilometers are not genetically distinct enough to be considered separate genetic populations. These results have important implications both for the identification of independent "populations" and in assessing the effect of scale in detecting patterns of genetic equilibrium and gene flow.

Extensive sampling of polar bears (Ursus maritimus) in the Northwest Passage (Canadian Arctic Archipelago) reveals population differentiation across multiple spatial and temporal scales.

As global warming accelerates the melting of Arctic sea ice, polar bears (Ursus maritimus) must adapt to a rapidly changing landscape. This process will necessarily alter the species distribution together with population dynamics and structure. Detailed knowledge of these changes is crucial to delineating conservation priorities. Here, we sampled 361 polar bears from across the center of the Canadian Arctic Archipelago spanning the Gulf of Boothia (GB) and M'Clintock Channel (MC). We use DNA microsatellites and mitochondrial control region sequences to quantify genetic differentiation, estimate gene flow, and infer population history. Two populations, roughly coincident with GB and MC, are significantly differentiated at both nuclear (F ST = 0.01) and mitochondrial (ΦST = 0.47; F ST = 0.29) loci, allowing Bayesian clustering analyses to assign individuals to either group. Our data imply that the causes of the mitochondrial and nuclear genetic patterns differ. Analysis of mtDNA reveals the matrilineal structure dates at least to the Holocene, and is common to individuals throughout the species' range. These mtDNA differences probably reflect both genetic drift and historical colonization dynamics. In contrast, the differentiation inferred from microsatellites is only on the scale of hundreds of years, possibly reflecting contemporary impediments to gene flow. Taken together, our data suggest that gene flow is insufficient to homogenize the GB and MC populations and support the designation of GB and MC as separate polar bear conservation units. Our study also provide a striking example of how nuclear DNA and mtDNA capture different aspects of a species demographic history.

Permanent genetic resources added to molecular ecology resources database 1 April 2013-31 May 2013.

This article documents the addition of 234 microsatellite marker loci to the Molecular Ecology Resources Database. Loci were developed for the following species: Acipenser sinensis, Aleochara bilineata, Aleochara bipustulata, Barbus meridionalis, Colossoma macropomum, Delia radicum, Drosophila nigrosparsa, Fontainea picrosperma, Helianthemum cinereum, Liomys pictus, Megabalanus azoricus, Pelteobagrus vachelli, Pleuragramma antarcticum, Podarcis hispanica type 1A, Sardinella brasiliensis and Sclerotinia homoeocarpa. These loci were cross-tested on the following species: Acipenser dabryanus, Barbus balcanicus, Barbus barbus, Barbus cyclolepis, Drosophila hydei, Drosophila melanogaster, Drosophila obscura, Drosophila subobscura, Fontainea australis, Fontainea fugax, Fontainea oraria, Fontainea rostrata, Fontainea venosa, Podarcis bocagei, Podarcis carbonelli, Podarcis liolepis, Podarcis muralis and Podarcis vaucheri.

Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrinus.

Peregrine falcon populations underwent devastating declines in the mid-20th century due to the bioaccumulation of organochlorine contaminants, becoming essentially extirpated east of the Great Plains and significantly reduced elsewhere in North America. Extensive re-introduction programs and restrictions on pesticide use in Canada and the United States have returned many populations to predecline sizes. A proper population genetic appraisal of the consequences of this decline requires an appropriate context defined by (i) meaningful demographic entities; and (ii) suitable reference populations. Here we explore the validity of currently recognized subspecies designations using data from the mitochondrial control region and 11 polymorphic microsatellite loci taken from 184 contemporary individuals from across the breeding range, and compare patterns of population genetic structure with historical patterns inferred from 95 museum specimens. Of the three North American subspecies, the west coast marine subspecies Falco peregrinus pealei is well differentiated genetically in both time periods using nuclear loci. In contrast, the partitioning of continental Falco peregrinus anatum and arctic Falco peregrinus tundrius subspecies is not substantiated, as individuals from these subspecies are historically indistinguishable genetically. Bayesian clustering analyses demonstrate that contemporary genetic differentiation between these two subspecies is mainly due to changes within F. p. anatum (specifically the southern F. p. anatum populations). Despite expectations and a variety of tests, no genetic bottleneck signature is found in the identified populations; in fact, many contemporary indices of diversity are higher than historical values. These results are rationalized by the promptness of the recovery and the possible introduction of new genetic material.

A TEST OF THE CHITTY HYPOTHESIS: INHERITANCE OF LIFE-HISTORY TRAITS IN MEADOW VOLES MICROTUS PENNSYLVANICUS.

The Chitty hypothesis proposes that the demographic changes occurring in microtine cycles are mediated by natural selection operating on the genetic composition of the population. Implicit in this hypothesis is the assumption that a suite of life-history traits is simultaneously undergoing selection and that these traits are strongly heritable. We tested this in two ways: first, by determining whether the year-to-year differences in phenotypes in fluctuating meadow vole populations in the field are maintained in samples of young animals raised in the laboratory, and second, whether the variation seen in the field has a heritable basis as determined by half-sib analysis. Parents were obtained in the springs of successive years from a fluctuating meadow vole population. These animals were bred in small field enclosures, and their progeny were raised in the laboratory. Animals raised in the laboratory differed significantly from those in the natural field population. In the field, young from the year when population size was increasing grew more rapidly than those from the peak year; in the laboratory, the opposite occurred. The ages at sexual maturity showed similar differences. Heritability analysis was performed on body weight, growth rate, and age and weight at sexual maturity. Virtually all these traits showed significant dam effects, but small or nonexistant sire effects. Thus, most of the variation was nongenetic in origin; maternal and other environmental effects were of overriding importance. We conclude that the heritabilities of these traits in nature are usually lower than necessary for natural selection to operate in the time frames characteristic of microtine cycles.

THE MITOCHONDRIAL AND NUCLEAR GENETIC HOMOGENEITY OF THE PHENOTYPICALLY DIVERSE DARWIN'S GROUND FINCHES.

The most extensively studied group of Darwin's finches is the genus Geospiza, the ground finches, and yet little is known about the evolutionary history and genetic relationships of these birds. Studies using either allozyme or morphological data have been unable to resolve relationships between the six species and numerous populations of ground finches. In this paper we report the results of a study using mitochondrial control region and nuclear internal transcribed spacer (ITS) 1 sequence data. The differentiation of the ground finch species based on morphological data is not reflected in either mitochondrial or nuclear DNA sequence phylogenies. Furthermore, there is little concordance between the mitochondrial haplotypes and ITS alleles found within individuals. We suggest that the absence of species-specific lineages can be attributed to ongoing hybridization involving all six species of Geospiza. There are no long term selective pressures against hybridization within this genus, and therefore a genetically homogenous genus may be maintained indefinitely. Hybridization has apparently played a role in the adaptive radiation of Darwin's finches.

MITOCHONDRIAL DNA HOMOGENEITY IN THE PHENOTYPICALLY DIVERSE REDPOLL FINCH COMPLEX (AVES: CARDUELINAE: CARDUELIS FLAMMEA-HORNEMANNI).

Breeding redpoll finches (Aves: Carduelinae) show extensive plumage and size variability and, in many cases, a plumage polymorphism that is not related to age or sex. This has been ascribed to extreme phenotypic variation within a single taxon or to moderate variability within distinct taxa coupled with hybridization. The predominant view favors the recognition of two largely sympatric species: Carduelis flammea, comprised of four well-marked subspecies-flammea, cabaret, islandica, and rostrata; and C. hornemanni, comprised of two subspecies-hornemanni and exilipes. We studied representative samples of these putative subspecies (except islandica) for variation in mitochondrial DNA (mtDNA). Using 20 informative restriction enzymes that recognized 124 sites (642 base pairs [bp] of sequence or ≈ 3.7% of the molecule), we identified 17 RFLP haplotypes in the 31 individuals surveyed. The haplotypes formed a simple phylogenetic network with most clones diverging by a single site difference from a common haplotype found in almost half of the individuals. Within populations and taxa, levels of mtDNA diversity were similar to those observed in other avian species. The pattern of mtDNA divergence among populations was statistically unrelated to their geographic or traditional taxonomic relationships, and the estimated distance between the two traditionally recognized species was very small relative to those typically observed among avian sister species.

Discordant temporal and geographic patterns in maternal lineages of eastern North American frogs, Rana catesbeiana (Ranidae) and Pseudacris crucifer (Hylidae).

Whether the Pleistocene has had a disproportionate impact on the recent diversification of temperate species, or played a lesser role in a more protracted process, has been a prominent evolutionary debate for the past decade. We used cytochrome b sequences to reconstruct the evolutionary histories of two widely co-distributed, and ecologically divergent frogs (Rana catesbeiana and Pseudacris crucifer) to examine the role of the Pleistocene in structuring these species. Results for R. catesbeiana reflect a pattern of allopatric fragmentation, likely in Coastal Plain refugia on either side of the Mississippi River dating to the mid to early Pleistocene. In contrast, P. crucifer contains numerous divergent lineages, including one west of the Mississippi River in the Interior Highlands, and in the east, multiple lineages that likely expanded from a number of southern Appalachian refugia with lineage sundering originating in the late Pliocene. Large-scale phylogeographic comparisons between these and other eastern North American species reflect both congruent and independent patterns of diversification, possibly reflecting the relative importance of dispersal ability and habitat associations. Although intra-lineage diversification has been structured by repeated Pleistocene glaciations, lineage sundering likely dates at least to the Pliocene in most (but not all) northern temperate amphibian and reptile species studied to date.

MICROGEOGRAPHIC VARIATION IN MITOCHONDRIAL DNA OF MEADOW VOLES (MICROTUS PENNSYLVANICUS) IN RELATION TO POPULATION DENSITY.

We examined mitochondrial-DNA (mtDNA) sequence heterogeneity on four adjacent trapping grids in an island population of meadow voles (Microtus pennsylvanicus) at two different population densities. Four restriction endonucleases revealed 20 different mtDNA composite phenotypes in samples totaling 198 meadow voles. There were significant heterogeneities in the distribution of four common mtDNA composite phenotypes among the four trapping grids, suggesting that there is population subdivision on a fine scale. Genetic distances between grids, mtDNA diversity within grids, and GST also varied during the study period. We found a decrease in genetic distance and an increase in diversity when the population density was high and vice versa when the population density was low. When population density was high, the coefficient of gene differentiation was smaller than the same coefficient observed when the population density was low. These changes in population subdivision and diversity are consistent with theoretical expectations of population structure in which effective female population size and dispersal are the critical variables. The data also support the hypothesis of maintenance of mtDNA diversity by population subdivision, rapid population growth rate, and dispersal.

The reproductive choices of eavesdropping female black-capped chickadees, Poecile atricapillus.

In animals where males engage in signalling interactions, females might evaluate male-male contests to inform their reproductive choices. We used interactive playback to engage territorial male black-capped chickadees (Poecile atricapillus) of known dominance status in countersinging contests with an aggressive or submissive opponent. Previous analysis of these data showed that high-ranking males who received aggressive playback were more likely to be cuckolded. Here we describe the particular reproductive decisions of females whose partners received aggressive versus submissive playback. The proportion of extra-pair young per brood was higher for females paired to high-ranking males that received aggressive playback compared to submissive playback, and similar to levels in broods of females paired to low-ranking males. We found no strong predictors of whether high-ranking subjects lost paternity following aggressive playback. Females usually preferred extra-pair sires with high dominance status. When females had extra-pair fertilizations with low-ranking males, females chose males who had received submissive playback. We conclude that females mated to aggressive-playback, high-ranking males pursued mixed mating strategies similar to those of females mated to low-ranking males. Our results support the idea that male performance in song contests may influence multiple aspects of female reproductive choices.

Genetic evidence for female-biased dispersal in the bullfrog, Rana catesbeiana (Ranidae).

Sex-biased dispersal is an important but unexplored area of amphibian ecology. We predicted female-biased dispersal in the bullfrog (Rana catesbeiana) based on aspects of their mating system and tested this prediction using data from seven polymorphic DNA microsatellite loci. Allelic (F-statistics) and genotypic [assignment index, (AIc)] frequencies from nine Ontario populations support our prediction, although significant sex differences in inbreeding and variance of AIc were not detected. The diversity of mating systems found in amphibians represents an important avenue for investigating the relationship between reproductive systems, dispersal and phylogeny.

Cryptic lineages in a small frog: the post-glacial history of the spring peeper, Pseudacris crucifer (Anura: Hylidae).

The spring peeper (Pseudacris crucifer) is believed to have been a primary herpetological invader of eastern North America following the most recent period of glacial retreat. We examined the phylogeographic pattern and population structure of P. crucifer to determine whether the distribution of haplotypic variants reflect post-Pleistocene recolonization dynamics. A number of geographically isolated evolutionary lineages were supported by both maximum parsimony and neighbor-joining analyses, and by coalescence approaches applied to mtDNA. South-western Ontario represents a high level of genotypic diversity (pi) due to the presence of two divergent lineages. The geographic distribution of these lineages are interpreted as reflecting post-glacial recolonization dynamics from separate, isolated refugia during the late Pleistocene that have come into secondary contact in SW Ontario. The phylogenetic placement of haplotypes from the range of P. crucifer bartramiana (Florida and South Carolina) does not allow for monophyly of P. crucifer crucifer, and therefore the bartramiana subspecies designation does not reflect a separate evolutionary lineage.