Rapid sperm evolution in the bluethroat (Luscinia svecica) subspecies complex

Spermatozoa are among the most variable animal cell types, and much research is currently directed towards explaining inter- and intraspecific variation in sperm form and function. Recent comparative studies in passerine birds have found associations between the level of sperm competition and both sperm length and sperm velocity. In species with sperm competition, postcopulatory sexual selection may shape the morphology of sperm as adaptations to the female environment. The speed of evolutionary change in sperm morphology at the species level is largely unknown. In this study, we analysed variation in sperm morphology among morphologically distinct and geographically isolated bluethroat subspecies in Europe. Consistent with previous studies, our analyses of mtDNA and nuclear introns suggest recent divergence and lack of lineage sorting among the subspecies. We found significant divergence in total sperm length and in the length of some sperm components (i.e. head and midpiece). There was a significantly positive relationship between pairwise divergences in sperm morphology and mitochondrial DNA, suggesting a role for genetic drift in sperm divergence. The magnitude of sperm length divergence was considerably higher than that in other geographically structured passerines, and even higher than that observed between several pairs of sister species. We hypothesize that the rapid sperm evolution in bluethroats is driven by sperm competition, and that strong postcopulatory sexual selection on sperm traits can lead to rapid speciation through reproductive incompatibilities.     

Joint Effects of Inbreeding and Local Adaptation on the Evolution of Genetic Load after Fragmentation

Abstract: Disruption of gene flow among demes after landscape fragmentation can facilitate local adaptation but increase the effect of genetic drift and inbreeding. The joint effects of these conflicting forces on the mean fitness of individuals in a population are unknown. Through simulations, we explored the effect of increased isolation on the evolution of genetic load over the short and long term when fitness depends in part on local adaptation. We ignored genetic effects on demography. We modeled complex genomes, where a subset of the loci were under divergent selection in different localities. When a fraction of the loci were under heterogeneous selection, isolation increased mean fitness in larger demes made up of hundreds of individuals because of improved local adaptation. In smaller demes of tens of individuals, increased isolation improved local adaptation very little and reduced overall fitness. Short‐term improvement of mean fitness after fragmentation may not be indicative of the long‐term evolution of fitness. Whatever the deme size and potential for local adaptation, migration of one or two individuals per generation minimized the genetic load in general. The slow dynamics of mean fitness following fragmentation suggests that conservation measures should be implemented before the consequences of isolation on the genetic load become of concern.     

Modeling biodiversity dynamics in countryside landscapes

The future of biodiversity hinges to a great extent on the conservation value of countryside, the growing fraction of Earth's surface heavily influenced by human activities. How many species, and which species, can persist in such landscapes (and analogous seascapes) are open questions. Here we explore two complementary theoretical frameworks to address these questions: species-area relationships and demographic models. We use the terrestrial mammal fauna of Central America to illustrate the application of both frameworks. We begin by proposing a multi-habitat species-area relationship, the countryside species-area relationship, to forecast species extinction rates. To apply it, we classify the mammal fauna by affinity to native and human-dominated habitats. We show how considering the conservation value of countryside habitats changes estimates derived from the classic species-area approach We also examine how the z value of the species-area relationship affects extinction estimates. Next, we present a framework for assessing the relative vulnerability of species to extinction in the countryside, based on the Skellam model of population dynamics. This model predicts the minimum area of contiguous native habitat required for persistence of a species, which we use as an indicator of vulnerability to habitat change. To apply the model, we use our habitat affinity classification of mammals and we estimate life-history parameters by species and habitat type. The resulting ranking of vulnerabilities is significantly correlated with the World Conservation Union (IUCN) Red List assessment.     

Detecting Biodiversity Hotspots by Species-Area Relationships: a Case Study of Mediterranean Beetles

Abstract:  Any method of identifying hotspots should take into account the effect of area on species richness. I examined the importance of the species-area relationship in determining tenebrionid (Coleoptera: Tenebrionidae) hotspots on the Aegean Islands (Greece). Thirty-two islands and 170 taxa (species and subspecies) were included in this study. I tested several species-area relationship models with linear and nonlinear regressions, including power, exponential, negative exponential, logistic, Gompertz, Weibull, Lomolino, and He-Legendre functions. Islands with positive residuals were identified as hotspots. I also analyzed the values of the C parameter of the power function and the simple species-area ratios. Species richness was significantly correlated with island area for all models. The power function model was the most convenient one. Most functions, however, identified certain islands as hotspots. The importance of endemics in insular biotas should be evaluated carefully because they are of high conservation concern. The simple use of the species-area relationship can be problematic when areas with no endemics are included. Therefore the importance of endemics should be evaluated according to different methods, such as percentages, to take into account different levels of endemism and different kinds of "endemics" (e.g., endemic to single islands vs. endemic to the archipelago). Because the species-area relationship is a key pattern in ecology, my findings can be applied at broader scales.     

A chemical trait creates a genetic trade-off between intra- and interspecific competitive ability

The importance of non-resource-based mechanisms of competition between plant species has been increasingly recognized, but little is known about how genetic variation and evolutionary changes in the underlying competitive traits might affect species coexistence. I found that genetic variation in sinigrin concentration, a putative allelopathic agent in Brassica nigra, affected the fitness of three heterospecific neighbor species but did not affect neighboring B. nigra individuals. Investment in sinigrin led to a negative genetic correlation between intra- and interspecific competitive ability, which over many generations could provide a strong stabilizing force maintaining both species and genetic diversity in this system.     

A quantitative genetic model of altruistic selection

Summary A quantitative genetic model for evolution by altruistic selection based on family selection models used in agricultural genetics is presented. A quantitative genetic version of Hamilton's rule is derived which indicates that evolution will proceed in an altruistic direction whenever the ratic of between-to within-family (or group) heritability exceeds the absolute value of the within-to between-family selection differential ratio. This ratio of heritabilities is equal to a ratio which includes only the phenotypic and genetic intraclass correlation coefficients, thus no heritabilities actually need to be estimated in determining the possibility of altruistic evolution. The phenotypic intraclass correlation can be estimated with standard analysis of variance methods. The genetic intraclass correlation may be estimated by the average within-group coefficient of relationship using genealogical data, by Wright's F-statistics using allele frequency data, or by a theoretical model based on a knowledge of interaction and mating patterns. Selection differentials may be measured by the regression of relative fitness, or one of its major components, on the phenotype of interest. Selection can be considered altruistic only if within-and between-family selection differentials have opposite signs. Consideration of empirical data on genetic and phenotypic intraclass correlations indicates that evolution may proceed in an altruistic direction even if the within-family selection differential exceeds the one between families, especially in situations in which pertinent environmental factors are randomly distributed among families.     

Two roads to two sexes: unifying gamete competition and gamete limitation in a single model of anisogamy evolution

Recent studies have revealed the importance of self-consistency in evolutionary models, particularly in the context of male–female interactions. This has been largely ignored in models of the ancestral divergence of the sexes, i.e., the evolution of anisogamy. Here, we model the evolution of anisogamy in a Fisher-consistent context, explicitly taking into account the number of interacting individuals in a typical reproductive group. We reveal an interaction between the number of adult individuals in the local mating group and the selection pressures responsible for the divergence of the sexes. The same underlying model can produce anisogamy in two different ways. Gamete competition can lead to anisogamy when it is relatively easy for gametes to find each other, but when this is more difficult and gamete competition is absent, gamete limitation can provide another route for anisogamy to evolve. In line with earlier models, organismal complexity favors anisogamy. We argue that the early contributions of Kalmus and Scudo, largely dismissed as group selectionist, are valid under certain conditions. Linking their work with the contributions of Parker helps to explain why precisely males keep producing more sperm than can ever lead to offspring: sperm could evolve to provision zygotes but this brings little profit for the effort required, because sperm would have to be equipped with provisioning ability before it is known which sperm will make it to the fertilization stage. This insight creates a logical link between paternal care under uncertain paternity (where again investment is selected against when some investment never brings about genetic benefits) and gamete size evolution.     

Evolving metacommunities: toward an evolutionary perspective on metacommunities

The metacommunity framework predicts that local coexistence depends on the outcome of local species interactions and regional migration. In analogous fashion, spatial structure among populations can shape species interactions through evolutionary mechanisms. Yet, most metacommunity theories assume that populations do not evolve. Here, we evaluate how evolution shapes local species coexistence and exclusion within the multiscale and multispecies context embodied by the metacommunity framework. In general, coexistence in joint ecological-evolutionary models requires low to intermediate dispersal rates that can promote maintenance of both regional species and genetic diversity. These conditions support a set of key mechanisms that modify patterns of species coexistence including local adaptation, gene storage effects, genetic rescue effects, spatial genetic subsidies, and metacommunity evolution. Multispecies extensions indicate that correlated selection can further alter the outcome of interspecific interactions depending on the magnitude and direction of correlations and shape of fitness trade-offs. We suggest that an evolving metacommunity perspective has the potential to generate novel predictions about community structure and function by incorporating the genetic and species diversity that characterize natural communities. In adopting such a perspective, we seek to facilitate understanding about the interactions between evolutionary and metacommunity dynamics.     

Area-Based Refinement for Selection of Reserve Sites with the Benefit-Function Approach

Abstract:  Optimization of resource use is necessary for efficient conservation planning. Many reserve-selection algorithms aim to identify representative but inexpensive networks, which may lead to selecting small sites due to their lower costs and collectively higher species richness. Nevertheless, larger sites would be preferable regarding species' long-term persistence. An area-based refinement can be used to overcome this problem. We used a reserve-planning framework in which continuous benefit functions valued representation (numbers of populations), and differential species weights were based on a species' local rarity and threatened status. We introduced a refinement based on the species-area relationship that provides relatively higher values for larger sites. We applied the proposed method to rich fen vegetation in southern Finland. The species-area refinement resulted in a network of significantly larger sites with minor trade-offs with representation (numbers of populations). Giving endangered species higher weights ensured that the trade-off occurred mostly between site size and representation of low-priority species. We recommend using a species-area refinement for practical, maximum-coverage conservation planning.     

A hidden species-area curve

The species-area curve, which describes the relationship between the number of observed species in a geographical region and the area of the region, plays a central role in biogeography. Beyond its scientific importance, the species-area curve is commonly used to assess the loss of species due to habitat loss. When the species-area curve is estimated from spatial samples, the existence of species with low or highly spatially variable abundance exaggerates the true rate at which species accumulate with area. Here, a hidden species-area curve is defined that accounts for this sampling effect and its estimation by maximum likelihood is outlined. Both the species-area curve and the hidden species-area curve are conditioned on the observed species list; thus the analysis does not depend on the total number of observed and unobserved species, that is, species richness. The method is tested by sub-sampling some tropical forest data and found to work well. It is also applied to a classic data set from the deep sea. For these data, accounting for this sampling effect has a large impact.     

A unified model of avian species richness on islands and continents

How many species in a given taxon should be found in a delimited area in a specified place in the world? Some recent literature suggests that the answer to this question depends strongly on the geographical, evolutionary, and ecological context. For example, current theory suggests that species accumulate as a function of area differently on continents and islands. Species richness-climate relationships have been examined separately on continents and on islands. This study tests the hypotheses that (1) the functional relationship between richness and climate is the same on continents and islands; (2) the species-area slope depends on distance-based isolation; (3) species-area relationships differ among land bridge islands, oceanic islands, and continents; (4) richness differs among biogeographic regions independently of climate and isolation. We related bird species numbers in a worldwide sample of 240 continental parcels and 346 islands to several environmental variables. We found that breeding bird richness varies similarly on islands and on continents as a function of mean annual temperature, an area x precipitation interaction, and the distance separating insular samples from the nearest continent (R2 = 0.86). Most studies to date have postulated that the slope of the species-area relationship depends upon isolation. In contrast, we found no such interaction. A richness-environment relationship derived using Old World sites accurately predicts patterns of richness in the New World and vice versa (R2 = 0.85). Our results suggest that most of the global variation in richness is not strongly context-specific; rather, it reflects a small number of general environmental constraints operating on both continents and islands.     

The immediate costs and long-term benefits of assisted gene flow in large populations

With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population-level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10–20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize—potentially too long for most climate-related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change.     

Evolution of self-organized division of labor in a response threshold model

Division of labor in social insects is determinant to their ecological success. Recent models emphasize that division of labor is an emergent property of the interactions among nestmates obeying to simple behavioral rules. However, the role of evolution in shaping these rules has been largely neglected. Here, we investigate a model that integrates the perspectives of self-organization and evolution. Our point of departure is the response threshold model, where we allow thresholds to evolve. We ask whether the thresholds will evolve to a state where division of labor emerges in a form that fits the needs of the colony. We find that division of labor can indeed evolve through the evolutionary branching of thresholds, leading to workers that differ in their tendency to take on a given task. However, the conditions under which division of labor evolves depend on the strength of selection on the two fitness components considered: amount of work performed and on worker distribution over tasks. When selection is strongest on the amount of work performed, division of labor evolves if switching tasks is costly. When selection is strongest on worker distribution, division of labor is less likely to evolve. Furthermore, we show that a biased distribution (like 3:1) of workers over tasks is not easily achievable by a threshold mechanism, even under strong selection. Contrary to expectation, multiple matings of colony foundresses impede the evolution of specialization. Overall, our model sheds light on the importance of considering the interaction between specific mechanisms and ecological requirements to better understand the evolutionary scenarios that lead to division of labor in complex systems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-012-1343-2) contains supplementary material, which is available to authorized users.     

Guidelines for genetic monitoring of translocated plant populations

Plant translocation is a useful tool for implementing assisted gene flow in recovery plans of critically endangered plant species. Although it helps to restore genetically viable populations, it is not devoid of genetic risks, such as poor adaptation of transplants and outbreeding depression in the hybrid progeny, which may have negative consequences in terms of demographic growth and plant fitness. Hence, a follow-up genetic monitoring should evaluate whether the translocated populations are genetically viable and self-sustaining in the short and long term. The causes of failure to adjust management responses also need to be identified. Molecular markers and fitness-related quantitative traits can be used to determine whether a plant translocation enhanced genetic diversity, increased fitness, and improved the probability of long-term survival. We devised guidelines and illustrated them with studies from the literature to help practitioners determine the appropriate genetic survey methods so that management practices can better integrate evolutionary processes. These guidelines include methods for sampling and for assessing changes in genetic diversity and differentiation, contemporary gene flow, mode of local recruitment, admixture level, the effects of genetic rescue, inbreeding or outbreeding depression and local adaptation on plant fitness, and long-term genetic changes.     

A model of ecological and evolutionary consequences of color polymorphism

We summarize direct and indirect effects on fitness components of animal color pattern and present a synthesis of theories concerning the ecological and evolutionary dynamics of chromatic multiple niche polymorphisms. Previous endeavors have aimed primarily at identifying conditions that promote the evolution and maintenance of polymorphisms. We consider in a conceptual model also the reciprocal influence of color polymorphism on population processes and propose that polymorphism entails selective advantages that may promote the ecological success of polymorphic species. The model begins with an evolutionary branching event from mono- to polymorphic condition that, under the influence of correlational selection, is predicted to promote the evolution of physical integration of coloration and other traits (cf. multi-trait coevolution and complex phenotypes). We propose that the coexistence within a population of alternative ecomorphs with coadapted gene complexes promotes utilization of diverse environmental resources, population stability and persistence, colonization success, and range expansions, and enhances the evolutionary potential and speciation. Conversely, we predict polymorphic populations to be less vulnerable to environmental change and at lower risk of range contractions and extinctions compared with monomorphic populations. We offer brief suggestions as to how these falsifiable predictions may be tested.     

Offspring size effects mediate competitive interactions in a colonial marine invertebrate

Over the past 30 years, numerous attempts to understand the relationship between offspring size and fitness have been made, and it has become clear that this critical relationship is strongly affected by environmental heterogeneity. For marine invertebrates, there has been a long-standing interest in the evolution of offspring size, but there have been very few empirical and theoretical examinations of post-metamorphic offspring size effects, and almost none have considered the effect of environmental heterogeneity on the offspring size/fitness relationship. We investigated the post-metamorphic effects of offspring size in the field for the colonial marine invertebrate Botrylloides violaceus. We also examined how the relationship between offspring size and performance was affected by three different types of intraspecific competition. We found strong and persistent effects of offspring size on survival and growth, but these effects depended on the level and type of intraspecific competition. Generally, competition strengthened the advantages of increasing maternal investment. Interestingly, we found that offspring size determined the outcome of competitive interaction: juveniles that had more maternal investment were more likely to encroach on another juvenile's territory. This suggests that mothers have the previously unrecognized potential to influence the outcome of competitive interactions in benthic marine invertebrates. We created a simple optimality model, which utilized the data generated from our field experiments, and found that increasing intraspecific competition resulted in an increase in predicted optimal size. Our results suggest that the relationship between offspring size and fitness is highly variable in the marine environment and strongly dependent on the density of conspecifics.     

The relationship between maternal phenotype and offspring quality: do older mothers really produce the best offspring?

Maternal effects are increasingly recognized as important drivers of population dynamics and determinants of evolutionary trajectories. Recently, there has been a proliferation of studies finding or citing a positive relationship between maternal size/age and offspring size or offspring quality. The relationship between maternal phenotype and offspring size is intriguing in that it is unclear why young mothers should produce offspring of inferior quality or fitness. Here we evaluate the underlying evolutionary pressures that may lead to a maternal size/age-offspring size correlation and consider the likelihood that such a correlation results in a positive relationship between the age or size of mothers and the fitness of their offspring. We find that, while there are a number of reasons why selection may favor the production of larger offspring by larger mothers, this change in size is more likely due to associated changes in the maternal phenotype that affect the offspring size-performance relationship. We did not find evidence that the offspring of older females should have intrinsically higher fitness. When we explored this issue theoretically, the only instance in which smaller mothers produce suboptimal offspring sizes is when a (largely unsupported) constraint on maximum offspring size is introduced into the model. It is clear that larger offspring fare better than smaller offspring when reared in the same environment, but this misses a critical point: different environments elicit selection for different optimal sizes of young. We suggest that caution should be exercised when interpreting the outcome of offspring-size experiments when offspring from different mothers are reared in a common environment, because this approach may remove the source of selection (e.g., reproducing in different context) that induced a shift in offspring size in the first place. It has been suggested that fish stocks should be managed to preserve these older age classes because larger mothers produce offspring with a greater chance of survival and subsequent recruitment. Overall, we suggest that, while there are clear and compelling reasons for preserving older females in exploited populations, there is little theoretical justification or evidence that older mothers produce offspring with higher per capita fitness than do younger mothers.     

Adaptive reversals in acid tolerance in copepods from lakes recovering from historical stress.

Anthropogenic habitat disturbance can often lead to rapid evolution of environmental tolerances in taxa that are able to withstand the stressor. What we do not understand, however, is how species respond when the stressor no longer exists, especially across landscapes and over a considerable length of time. Once anthropogenic disturbance is removed and if there is an ecological trade-off associated with local adaptation to such an historical stressor, then evolutionary theory would predict evolutionary reversals. On the Boreal Shield, tens of thousands of lakes acidified as a result of SO2 emissions, but many of these lakes are undergoing chemical recovery as a consequence of reduced emissions. We investigated the adaptive consequences of disturbance and recovery to zooplankton living in these lakes by asking (1) if contemporary evolution of acid tolerance had arisen among Leptodiaptomus minutus copepod populations in multiple circum-neutral lakes with and without historical acidification, (2) if L. minutus populations were adaptively responding to reversals in selection in historically acidified lakes that had recovered to pH 6.0 for at least 6-8 years, and (3) if there was a fitness trade-off for L. minutus individuals with high acid tolerance at circum-neutral pH. L. minutus populations had higher acid tolerances in circum-neutral lakes with a history of acidification than in local and distant lakes that were never acidified. However, copepods in circum-neutral acid-recovering lakes were less acid-tolerant than were copepods in lakes with longer recovery time. This adaptive reversal in acid tolerance of L. minutus populations following lake recovery was supported by the results of a laboratory experiment that indicated a fitness trade-off in copepods with high acid tolerances at circum-neutral pH. These responses appear to have a genetic basis and suggest that L. minutus is highly adaptive to changes in environmental conditions. Therefore, restoration managers should focus on removing environmental stressors, and adaptable species will be able to reverse evolutionary responses to environmental disturbance in the years following recovery.     

Conservation Genetics in the Management of Desert Fishes

Abstract: The status and security of fishes in North American deserts have steadily declined in this century due to man's activities in this naturally fragile region. We address genetic aspects of the population structure of desert fishes as applicable to conservation and recovery programs by developing two zoogeographic models of isolation and gene flow. In the Death Valley model populations are isolated, with no chance of natural gene flow among them. Genetic diversity within populations tends to be low, but genetic divergence among populations within a species is high. In the Stream Hierarchy model, a complicated hierarchical genetic structure exists and is a function of geographic proximity and connectivity of habitats. Within-habitat genetic diversity tends to be higher, and among-habitat differentiation lower, than in the Death Valley model. These two systems must be recognized as distinct and managed differently. We also suggest three areas of experimentation needed to better understand and manage genetic stocks of desert fishes: relationships between heterozygosity and fitness, experimental mixing of similar stocks to examine effects of increased heterozygosity, and analysis of the relative roles of genetic adaptation and phenotypic plasticity in local differentiation.     

The consequences of genetic diversity in competitive communities

Several lines of evidence suggest that the species diversity and composition of communities should depend on genetic diversity within component species, but there has been very little effort to directly assess this possibility. Here I use models of competition among genotypes and species to demonstrate a strong positive effect of the number of genotypes per species on species diversity across a range of conditions. Genetic diversity allows species to respond to selection imposed by competition, resulting in both functional convergence and divergence among species depending on their initial niche positions. This ability to respond to selection promotes species coexistence and contributes to a reduction in variation in species composition among communities. These models suggest that whenever individual fitness depends on the degree of functional similarity between a focal individual and its competitors, genetic diversity should promote species coexistence; this prediction is consistent with the few relevant empirical data collected to date. The results point to the importance of considering the genetic origin and diversity of material used in ecological experiments and in restoration efforts, in addition to highlighting potentially important community consequences of the loss of genetic diversity in natural populations.