Multigenerational Fitness Effects of Natural Immigration Indicate Strong Heterosis and Epistatic Breakdown in a Wild Bird Population.

AbstractThe fitness of immigrants and their descendants produced within recipient populations fundamentally underpins the genetic and population dynamic consequences of immigration. Immigrants can in principle induce contrasting genetic effects on fitness across generations, reflecting multifaceted additive, dominance, and epistatic effects. Yet full multigenerational and sex-specific fitness effects of regular immigration have not been quantified within naturally structured systems, precluding inference on underlying genetic architectures and population outcomes. We used four decades of song sparrow (Melospiza melodia) life history and pedigree data to quantify fitness of natural immigrants, natives, and their F1, F2, and backcross descendants and test for evidence of nonadditive genetic effects. Values of key fitness components (including adult lifetime reproductive success and zygote survival) of F1 offspring of immigrant-native matings substantially exceeded their parent mean, indicating strong heterosis. Meanwhile, F2 offspring of F1-F1 matings had notably low values, indicating surprisingly strong epistatic breakdown. Furthermore, magnitudes of effects varied among fitness components and differed between female and male descendants. These results demonstrate that strong nonadditive genetic effects on fitness can arise within weakly structured and fragmented populations experiencing frequent natural immigration. Such effects will substantially affect the net degree of effective gene flow and resulting local genetic introgression and adaptation.

Patterns and effects of gene flow on adaptation across spatial scales: implications for management.

Gene flow can have rapid effects on adaptation and is an important evolutionary tool available when undertaking biological conservation and restoration. This tool is underused partly because of the perceived risk of outbreeding depression and loss of mean fitness when different populations are crossed. In this article, we briefly review some theory and empirical findings on how genetic variation is distributed across species ranges, describe known patterns of gene flow in nature with respect to environmental gradients, and highlight the effects of gene flow on adaptation in small or stressed populations in challenging environments (e.g., at species range limits). We then present a case study involving crosses at varying spatial scales among mountain populations of a trigger plant (Stylidium armeria: Stylidiaceae) in the Australian Alps to highlight how some issues around gene flow effects can be evaluated. We found evidence of outbreeding depression in seed production at greater geographic distances. Nevertheless, we found no evidence of maladaptive gene flow effects in likelihood of germination, plant performance (size), and performance variance, suggesting that gene flow at all spatial scales produces offspring with high adaptive potential. This case study demonstrates a path to evaluating how increasing sources of gene flow in managed wild and restored populations could identify some offspring with high fitness that could bolster the ability of populations to adapt to future environmental changes. We suggest further ways in which managers and researchers can act to understand and consider adaptive gene flow in natural and conservation contexts under rapidly changing conditions.

Optimal outbreeding is shaped during larval life-history in the splash pool copepod Tigriopus californicus.

Inbreeding and outbreeding depression are dynamic forms of selection critical to mating system evolution and the efficacy of conservation biology. Most evidence on how the relative severity and timing of these forces are shaped is confined to self-fertilization, distant outcrossing, and intermediate 'optimal outcrossing' in hermaphrodites. We tested the notion that closed population demographics may reduce and delay the costs of inbreeding relative to distant outbreeding in an intertidal copepod with separate sexes and a biphasic larval / post-metamorphic life-history (Tigriopus californicus). At three lifecycle stages (fecundity, metamorphosis, and post-metamorphosis), we quantified the effects of inbreeding and outbreeding in crosses with varying degrees of recent common ancestry. Although inbreeding and outbreeding depression have distinct genetic mechanisms, both manifested the same stage-specific consequences for fitness. Inbreeding and outbreeding depression were not apparent for fecundity, post-metamorphic survival, sex ratio, or the ability to acquire mates, but inbreeding between full siblings and outbreeding between interpopulation hybrids reduced the fraction of offspring that completed metamorphosis by 32% and 47%, respectively. On average, the effects of inbreeding on metamorphic rate were weaker and nearly twice as variable among families than those of outbreeding, suggesting genetic load was less pervasive than the incompatibilities accrued between divergent populations. Overall, our results indicate the transition from larval to juvenile life stages is markedly susceptible to both inbreeding and outbreeding depression in T. californicus. We suggest stage-specific selection acting concurrently with the timing of metamorphosis may be an instrumental factor shaping reproductive optima in species with complex life-histories.

The conservation value of small population remnants: variability in inbreeding depression and heterosis of a perennial herb, the narrow-leaved purple coneflower (Echinacea angustifolia).

Anthropogenically fragmented populations may have reduced fitness due to loss of genetic diversity and inbreeding. The extent of such fitness losses due to fragmentation and potential gains from conservation actions are infrequently assessed together empirically. Controlled crosses within and among populations can identify whether populations are at risk of inbreeding depression and whether interpopulation crossing alleviates fitness loss. Because fitness depends on environment and life stage, studies quantifying cumulative fitness over a large portion of the lifecycle in conditions that mimic natural environments are most informative. To assess fitness consequences of habitat fragmentation, we leveraged controlled within-family, within-population, and between-population crosses to quantify inbreeding depression and heterosis in seven populations of Echinacea angustifolia within a 6400-hectare area. We then assessed cumulative offspring fitness after 14 years of growth in a natural experimental plot (N = 1136). Mean fitness of progeny from within-population crosses varied considerably, indicating genetic differentiation among source populations, even though these sites are all less than 9 km apart. The fitness consequences of within-family and between-population crosses varied in magnitude and direction. Only one of the seven populations showed inbreeding depression of high effect, while four populations showed substantial heterosis. Outbreeding depression was rare and slight. Our findings indicate that local crossings between isolated populations yield unpredictable fitness consequences ranging from slight decreases to substantial increases. Interestingly, inbreeding depression and heterosis did not relate closely to population size, suggesting that all fragmented populations could contribute to conservation goals as either pollen recipients or donors.

Can heterosis and inbreeding depression explain the maintenance of outcrossing in a cleistogamous perennial?

PREMISE: What maintains mixed mating is an evolutionary enigma. Cleistogamy-the production of both potentially outcrossing chasmogamous and obligately selfing cleistogamous flowers on the same individual plant-is an excellent system to study the costs of selfing. Inbreeding depression can prevent the evolution of greater selfing within populations, and heterosis in crosses between populations may further tip the balance in favor of outcrossing. Few empirical estimates of inbreeding depression and heterosis in the same system exist for cleistogamous species. METHODS: We investigate the potential costs of selfing by quantifying inbreeding depression and heterosis in three populations of the cleistogamous perennial Ruellia humilis Nutt (Acanthaceae). We performed three types of hand-pollinations-self, outcross-within, and outcross-between populations-and measured seed number, germination, total flower production, and estimated cumulative fitness for the resulting progeny in a greenhouse experiment. RESULTS: We found moderate inbreeding depression for cumulative fitness (<30%) in two populations, but outbreeding depression for crosses within a third population (-26%). For between-population crosses, there was weak to modest heterosis (11-47%) in two of the population combinations, but modest to strong outbreeding depression (-21 to -71%) in the other four combinations. CONCLUSIONS: Neither inbreeding depression nor heterosis was of sufficient magnitude to explain the continued production of chasmogamous flowers given the relative energetic advantage of cleistogamous flowers previously estimated for these populations. Outbreeding depression either within or between populations makes the maintenance of chasmogamous flowers even harder to explain. More information is needed on the genetic basis of cleistogamy to resolve this conundrum.

PREMISA: Lo que mantiene los sistemas de apareamiento mixto aún es un enigma. La cleistogamia, la producción de flores con potencial de cruzamiento casmógamas, y de flores cleistógamas obligadamente autofecundadas en la misma planta, es un excelente sistema para estudiar los costos de la autofecundación. La depresión endogámica puede prevenir la evolución hacia una mayor autofecundación dentro de las poblaciones, y la heterosis de los cruces entre poblaciones puede inclinar aún más la balanza a favor del cruzamiento. Existen pocas estimaciones empíricas de depresión endogámica y heterosis en el mismo sistema para especies cleistógamas. MÉTODOS: Investigamos los costos potenciales de la autofecundación cuantificando la depresión endogámica y la heterosis en tres poblaciones de la perenne cleistógama Ruellia humilis Nutt (Acanthaceae). Realizamos autopolinizaciones manuales, y cruces dentro y entre poblaciones, Medimos el número de semillas, la germinación, la producción total de flores y estimamos la acumulación de fitness para la progenie resultante en un experimento de invernadero. RESULTADOS: Encontramos depresión endogámica moderada para fitness acumulado (<30%) en dos poblaciones, pero depresión exogámica para cruces dentro de la tercera población (-26%). Entre cruces de población, hubo heterosis de débil a modesta (11-47%) en dos de las combinaciones de poblaciones, pero depresión exogámica moderada a fuerte (-21 a -71%) en las otras cuatro combinaciones. CONCLUSIONES: Ni la depresión endogámica, ni la heterosis fueron de suficiente magnitud para explicar la producción continua de flores casmógamas dada la ventaja energética relativa de las flores cleistógamas previamente estimadas para estas poblaciones. La depresión exogámica, ya sea dentro o entre poblaciones, hace que el mantenimiento de las flores casmógamas sea aún más difícil de explicar. Se necesita más información sobre la base genética de la cleistogamia para resolver este enigma.

Expansion of the rare Eucalyptus risdonii under climate change through hybridization with a closely related species despite hybrid inferiority.

BACKGROUND AND AIMS: Hybridization is increasingly recognized as an integral part of the dynamics of species range expansion and contraction. Thus, it is important to understand the reproductive barriers between co-occurring species. Extending previous studies that argued that the rare Eucalyptus risdonii was expanding into the range of the surrounding E. amygdalina by both seed and pollen dispersal, we here investigate the long-term fitness of both species and their hybrids and whether expansion is continuing. METHODS: We assessed the survival of phenotypes representing a continuum between the two pure species in a natural hybrid swarm after 29 years, along with seedling recruitment. The performance of pure species as well as of artificial and natural hybrids was also assessed over 28 years in a common garden trial. KEY RESULTS: In the hybrid zone, E. amygdalina adults showed greater mortality than E. risdonii, and the current seedling cohort is still dominated by E. risdonii phenotypes. Morphologically intermediate individuals appeared to be the least fit. Similar results were observed after growing artificial first-generation and natural hybrids alongside pure species families in a common garden trial. Here, the survival, reproduction, health and growth of the intermediate hybrids were significantly less than those of either pure species, consistent with hybrid inferiority, although this did not manifest until later reproductive ages. Among the variable progeny of natural intermediate hybrids, the most E. risdonii-like phenotypes were the most fit. CONCLUSIONS: This study contributes to the increasing number of reports of hybrid inferiority in Eucalyptus, suggesting that post-zygotic barriers contribute to the maintenance of species integrity even between closely related species. However, with fitness rapidly recovered following backcrossing, it is argued that hybridization can still be an important evolutionary process, in the present case appearing to contribute to the range expansion of the rare E. risdonii in response to climate change.

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.

Directrices para el Monitoreo Genético de Poblaciones de Plantas Translocadas Resumen La translocación de plantas es una herramienta útil para implementar el flujo génico asistido en los planes de recuperación de especies de plantas en peligro crítico. Aunque ayuda a restaurar poblaciones genéticamente viables, no está exento de riesgos genéticos, como la baja adaptación de los trasplantes y la depresión por exogamia en la progenie híbrida, que pueden tener consecuencias negativas en términos de crecimiento demográfico y adaptabilidad de las plantas. Por tanto, un monitoreo genético de seguimiento debería evaluar si las poblaciones translocadas son genéticamente viables y autosustentables en el corto y largo plazos. Las causas del fracaso al ajustar respuestas de manejo también deben ser identificadas. Se pueden utilizar marcadores moleculares y atributos relacionados con la adaptabilidad para determinar si una translocación de plantas aumentó la diversidad genética, incrementó la adaptabilidad y mejoró la probabilidad de supervivencia a largo plazo. Diseñamos directrices y las ilustramos con estudios en la literatura para ayudar a que los practicantes determinen los métodos de monitoreo genético adecuados para que las prácticas de manejo integren procesos evolutivos de mejor manera. Estas directrices incluyen métodos para muestrear y evaluar cambios en la diversidad y diferenciación genética; el flujo génico contemporáneo; la forma de reclutamiento local; el nivel de mezcla; los efectos del rescate genético, la depresión por endogamia o exogamia y la adaptación local sobre la adaptabilidad de las plantas y los cambios genéticos a largo plazo.

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.

Con el deterioro de la salud genética de muchas poblaciones de plantas y animales debido a la ventaja que le lleva el cambio climático a la adaptación, algunas intervenciones, como el flujo génico asistido (FGA), pueden proporcionar la variación genética necesaria para que las poblaciones se adapten al cambio climático. Simulamos diferentes escenarios de FGA aplicado en poblaciones grandes y medimos los resultados en la aptitud a nivel poblacional para determinar las circunstancias en las que merece la pena realizar FGA. Cuando no hubo depresión endogámica, el FGA produjo un beneficio en pocas generaciones sólo cuando se introdujeron genotipos que tenían una aptitud mucho mayor que los individuos locales y cuando unos cuantos genes de gran efecto controlaron los rasgos que afectaban a la aptitud. El flujo génico asistido fue dañino en periodos cortos (p.ej.: las primeras 10-20 generaciones) si existía una fuerte depresión exogámica o una variación genética deletérea introducida. Cuando muchos loci de pequeño efecto controlaron el rasgo adaptativo, los beneficios del FGA tardaron más de 10 generaciones en aparecer - un tiempo potencialmente muy largo para la mayoría de la gestión relacionada con el clima. La integridad genómica de la población receptora casi siempre permaneció intacta después del FGA; es decir, la cantidad de material genético de la población donante generalmente no constituyó más que la fracción de población introducida en el genoma de la población receptora. La rotación genómica significativa (p.ej.: reemplazos >50%) sólo ocurrió cuando la ventaja selectiva del rasgo adaptativo y la fracción de reubicación fueron extremadamente elevadas. Nuestros resultados serán útiles cuando se use la gestión adaptativa para mantener la salud genética y la productividad de las poblaciones grandes bajo el cambio climático.

The ecological causes and consequences of hard and soft selection.

Interactions between natural selection and population dynamics are central to both evolutionary-ecology and biological responses to anthropogenic change. Natural selection is often thought to incur a demographic cost that, at least temporarily, reduces population growth. However, hard and soft selection clarify that the influence of natural selection on population dynamics depends on ecological context. Under hard selection, an individual's fitness is independent of the population's phenotypic composition, and substantial population declines can occur when phenotypes are mismatched with the environment. In contrast, under soft selection, an individual's fitness is influenced by its phenotype relative to other interacting conspecifics. Soft selection generally influences which, but not how many, individuals survive and reproduce, resulting in little effect on population growth. Despite these important differences, the distinction between hard and soft selection is rarely considered in ecology. Here, we review and synthesize literature on hard and soft selection, explore their ecological causes and implications and highlight their conservation relevance to climate change, inbreeding depression, outbreeding depression and harvest. Overall, these concepts emphasise that natural selection and evolution may often have negligible or counterintuitive effects on population growth-underappreciated outcomes that have major implications in a rapidly changing world.

Evaluating the outcomes of genetic rescue attempts.

Augmenting gene flow is a powerful tool for the conservation of small, isolated populations. However, genetic rescue attempts have largely been limited to populations at the brink of extinction, in part due to concerns over negative outcomes (e.g., outbreeding depression). Increasing habitat fragmentation may necessitate more proactive genetic management. Broader application of augmented gene flow will, in turn, require rigorous evaluation to increase confidence and identify pitfalls in this approach. To date, there has been no assessment of best monitoring practices for genetic rescue attempts. We used genomically explicit, individual-based simulations to examine the effectiveness of common approaches (i.e., tests for increases in fitness, migrant ancestry, heterozygosity, and abundance) for determining whether genetic rescue or outbreeding depression occurred. Statistical power to detect the effects of gene flow on fitness was high (≥0.8) when effect sizes were large, a finding consistent with those from previous studies on severely inbred populations. However, smaller effects of gene flow on fitness can appreciably affect persistence probability but current evaluation approaches fail to provide results from which reliable inferences can be drawn. The power of the metrics we examined to evaluate genetic rescue attempts depended on the time since gene flow and whether gene flow was beneficial or deleterious. Encouragingly, the use of multiple metrics provided nonredundant information and improved inference reliability, highlighting the importance of intensive monitoring efforts. Further development of best practices for evaluating genetic rescue attempts will be crucial for a responsible transition to increased use of translocations to decrease extinction risk.

Evaluación de los Resultados de los Intentos de Rescate Genético Resumen El aumento del flujo génico es una herramienta poderosa para la conservación de poblaciones pequeñas y aisladas. Sin embargo, los intentos de rescate genético en su mayoría se han limitado a las poblaciones que se encuentran al borde de la extinción, en parte debido a la preocupación que existe por los resultados negativos (es decir, la depresión exogámica). La creciente fragmentación del hábitat puede requerir un manejo genético más proactivo. La aplicación más extensa del flujo génico aumentado requerirá a su vez una evaluación rigurosa para incrementar la confianza e identificar las dificultades de esta estrategia. A la fecha, no ha habido una evaluación de las mejores prácticas de monitoreo para los intentos de rescate genético. Usamos simulaciones explícitas basadas en individuos para examinar la efectividad de las estrategias comunes (es decir, análisis del incremento en adaptabilidad, ascendencia migratoria, heterocigosidad y abundancia) para determinar si ocurrió el rescate genético o la depresión exogámica. El poder estadístico para detectar los efectos del flujo génico sobre la adaptabilidad fue elevado (≥0.8) cuando el tamaño de los efectos fue grande, un hallazgo consistente con aquellos realizados en estudios previos sobre poblaciones con una endogamia severa. Sin embargo, los efectos menores del flujo génico sobre la adaptabilidad pueden afectar de manera apreciable la probabilidad de persistencia, pero las estrategias actuales de evaluación no proporcionan resultados de los cuales se puedan hacer inferencias confiables. El poder de las medidas que examinamos para evaluar los intentos de rescate genético dependió del tiempo desde que inició el flujo génico y de si el flujo génico fue benéfico o perjudicial. De manera alentadora, el uso de múltiples medidas proporcionó información no redundante y mejoró la confiabilidad de la inferencia, resaltando así la importancia de los esfuerzos intensivos de monitoreo. El futuro desarrollo de mejores prácticas para la evaluación de los intentos de rescate genético será de suma importancia para la transición responsable hacia el mayor uso de reubicaciones para reducir el riesgo de extinción.

Negative effects of individual heterozygosity on reproductive success in a wild bird population.

The evolutionary consequences of individual genetic diversity are frequently studied by assessing heterozygosity-fitness correlations (HFCs). The prevalence of positive and negative HFCs and the predominance of general versus local effects in wild populations are far from understood, partly because comprehensive studies testing for both inbreeding and outbreeding depression are lacking. We studied a genetically diverse population of blue tits in southern Germany using a genome-wide set of 87 microsatellites to investigate the relationship between proxies of reproductive success and measures of multilocus and single-locus individual heterozygosity (MLH and SLH). We used complimentary measures of MLH and partitioned markers into functional categories according to their position in the blue tit genome. HFCs based on MLH were consistently negative for functional loci, whereas correlations were rather inconsistent for loci found in nonfunctional areas of the genome. Clutch size was the only reproductive variable showing a general effect. We found evidence for local effects for three measures of reproductive success: arrival date at the breeding site, the probability of breeding at the study site and male reproductive success. For these, we observed consistent, and relatively strong, negative effects at one functional locus. Remarkably, this marker had a similar effect in another blue tit population from Austria (~400 km to the east). We suggest that a genetic local effect on timing of arrival might be responsible for most negative HFCs detected, with carry-over effects on other reproductive traits. This effect could reflect individual differences in the distance between overwintering areas and breeding sites.

Heterozygosity-Fitness Correlations in a Continental Island Population of Thorn-Tailed Rayadito.

Heterozygosity-fitness correlations (HFCs) have been used to monitor the effects of inbreeding in threatened populations. HFCs can also be useful to investigate the potential effects of inbreeding in isolated relict populations of long-term persistence and to better understand the role of inbreeding and outbreeding as drivers of changes in genetic diversity. We studied a continental island population of thorn-tailed rayadito (Aphrastura spinicauda) inhabiting the relict forest of Fray Jorge National Park, north-central Chile. This population has experienced a long-term, gradual process of isolation since the end of the Tertiary. Using 10 years of field data in combination with molecular techniques, we tested for HFCs to assess the importance of inbreeding depression. If inbreeding depression is important, we predict a positive relationship between individual heterozygosity and fitness-related traits. We genotyped 183 individuals at 12 polymorphic microsatellite loci and used 7 measures of reproductive success and estimates of apparent survival to calculate HFCs. We found weak to moderate statistical support (P-values between 0.05 and 0.01) for a linear effect of female multi-locus heterozygosity (MLH) on clutch size and nonlinear effects on laying date and fledging success. While more heterozygous females laid smaller clutches, nonlinear effects indicated that females with intermediate values of MLH started laying earlier and had higher fledging success. We found no evidence for effects of MLH on annual fecundity or on apparent survival. Our results along with the long-term demographic stability of the study population contradict the hypothesis that inbreeding depression occurs in this population.

Heterosis is common and inbreeding depression absent in natural populations of Arabidopsis thaliana.

The importance of genetic drift in shaping patterns of adaptive genetic variation in nature is poorly known. Genetic drift should drive partially recessive deleterious mutations to high frequency, and inter-population crosses may therefore exhibit heterosis (increased fitness relative to intra-population crosses). Low genetic diversity and greater genetic distance between populations should increase the magnitude of heterosis. Moreover, drift and selection should remove strongly deleterious recessive alleles from individual populations, resulting in reduced inbreeding depression. To estimate heterosis, we crossed 90 independent line pairs of Arabidopsis thaliana from 15 pairs of natural populations sampled across Fennoscandia and crossed an additional 41 line pairs from a subset of four of these populations to estimate inbreeding depression. We measured lifetime fitness of crosses relative to parents in a large outdoor common garden (8,448 plants in total) in central Sweden. To examine the effects of genetic diversity and genetic distance on heterosis, we genotyped parental lines for 869 SNPs. Overall, genetic variation within populations was low (median expected heterozygosity = 0.02), and genetic differentiation was high (median FST  = 0.82). Crosses between 10 of 15 population pairs exhibited significant heterosis, with magnitudes of heterosis as high as 117%. We found no significant inbreeding depression, suggesting that the observed heterosis is due to fixation of mildly deleterious alleles within populations. Widespread and substantial heterosis indicates an important role for drift in shaping genetic variation, but there was no significant relationship between fitness of crosses relative to parents and genetic diversity or genetic distance between populations.

Conservation practitioners' understanding of how to manage evolutionary processes.

Both academics and practitioners consider a lack of knowledge about evolutionary theory to be a general barrier to effectively managing genetic diversity. However, it is challenging to judge practitioners' level of understanding and how this influences their management decisions. Knowledge built through experience may be difficult for practitioners to articulate, but could nonetheless result in appropriate management strategies. To date, researchers have assessed only the explicit (formal) knowledge practitioners have of evolutionary concepts. To explore practitioners' understanding of evolutionary concepts, it is necessary to consider how they might apply explicit and implicit knowledge to their management decisions. Using an online survey, we asked Australian practitioners to respond to 2 common management scenarios in which there is strong evidence that managing genetic diversity can improve outcomes: managing small, isolated populations and sourcing seeds for restoration projects. In describing their approach to these scenarios, practitioners demonstrated a stronger understanding of the effective management of genetic diversity than the definitions of the relevant concepts. However, their management of genetic diversity within small populations was closer to best practice than for restoration projects. Moreover, the risks practitioners described in implementing best practice management were more likely to affect their approach to restoration than translocation projects. These findings provide evidence that strategies to build the capacity of practitioners to manage genetic diversity should focus on realistic management scenarios. Given that practitioners recognize the importance of adapting their practices and the strong evidence for the benefits of actively managing genetic diversity, there is hope that better engagement by evolutionary biologists with practitioners could facilitate significant shifts toward evolutionarily enlightened management.

Entendimiento de los Practicantes de la Conservación sobre Cómo Manejar los Procesos Evolutivos Resumen Tanto los académicos como los practicantes consideran que una falta de conocimiento sobre la teoría evolutiva es una barrera general para el manejo efectivo de la diversidad genética. Sin embargo, es complicado juzgar el nivel de entendimiento de los practicantes y cómo éste influye sobre sus decisiones de manejo. El conocimiento construido por medio de la experiencia puede ser difícil de articular para los practicantes, pero de igual manera podría resultar en estrategias adecuadas de manejo. A la fecha, los investigadores han evaluado solamente el conocimiento explícito (formal) que tienen los practicantes sobre los conceptos evolutivos. Para explorar el entendimiento que tienen los practicantes sobre los conceptos evolutivos es necesario considerar cómo podrían aplicar conocimientos explícitos e implícitos a sus decisiones de manejo. Por medio de una encuesta en línea, le pedimos a practicantes australianos que respondieran a dos escenarios comunes de manejo en los cuales hay fuertes evidencias de que el manejo de la diversidad genética puede mejorar los resultados: el manejo de poblaciones pequeñas y aisladas, y la obtención de semillas para proyectos de restauración. Cuando describieron sus métodos para estos escenarios, los practicantes demostraron tener un entendimiento más completo del manejo efectivo de la diversidad genética que de las definiciones de los conceptos relevantes. Sin embargo, su manejo de la diversidad genética dentro de poblaciones pequeñas estuvo más cerca de la mejor práctica que para los proyectos de restauración. Además, los riesgos que los practicantes describieron en la implementación del manejo de la mejor práctica tuvieron una mayor probabilidad de afectar a sus estrategias de restauración que a las de reubicación. Estos resultados proporcionan evidencia de que las estrategias para construir la capacidad de los practicantes para manejar la diversidad genética deben enfocarse en escenarios realistas de manejo. Ya que los practicantes reconocen la importancia de adaptar sus prácticas y reconocen la sólida evidencia para los beneficios del manejo activo de la diversidad genética, hay esperanzas de que una mejor colaboración entre los practicantes y los biólogos evolutivos pudiera facilitar cambios significativos hacia un manejo informado evolutivamente.

Local adaptation of phenology revealed in outcrosses between spawning segments of a salmonid population.

Local adaptation has been demonstrated in spatially or temporally distant animal populations but seldom in proximate populations. To address the scale of local adaptation in Pacific salmon (Oncorhynchus spp.), two generations of hybrids between temporally separated spawning segments were made in a population of pink salmon (O. gorbuscha) and compared with controls to evaluate the genetic architecture underlying adult migration time and to test for declines in marine survival that resulted from outbreeding depression. Bayesian mixed-effects models revealed that adult migration times in hybrid lines were intermediate to those of controls and that additive sources of genetic variation were significant, thereby indicating that local adaptation has acted on additive genetic variation in shaping this trait. Similarly, a line cross analysis revealed that an additive model best described the genetic architecture of adult migration time. In contrast, marine survival was generally similar between control and hybrid lines, which suggested that the effect of outbreeding upon marine survival was minimal at such a fine scale of genetic divergence. The implications of these results are that (a) local adaptation can facilitate genetic divergence of life history traits between proximate subpopulations; (b) artificial relaxation of natural barriers to gene flow can cause maladaptive shifts in life history traits; and (c) wild populations may harbour fine-scale adaptive variation that supports productivity and sustainability.

Balancing in- and out-breeding by the predatory mite Phytoseiulus persimilis.

In- and out-breeding depressions are commonly observed phenomena in sexually reproducing organisms with a patchy distribution pattern, and spatial segmentation and/or isolation of groups. At the genetic level, inbreeding depression is due to increased homozygosity, whereas outbreeding depression is due to inferior genetic compatibility of mates. Optimal outbreeding theory suggests that intermediate levels of mate relatedness should provide for the highest fitness gains. Here, we assessed the fitness consequences of genetic relatedness between mates in plant-inhabiting predatory mites Phytoseiulus persimilis, which are obligatory sexually reproducing but haplo-diploid. Both females and males arise from fertilized eggs but males lose the paternal chromosome set during embryogenesis, dubbed pseudo-arrhenotoky. Phytoseiulus persimilis are highly efficacious in reducing crop-damaging spider mite populations and widely used in biological control. Using iso-female lines of two populations, from Sicily and Greece, we assessed the fecundity of females, and sex ratio of their offspring, that mated with either a sibling, a male from the same population or a male from the other population. Additionally, we recorded mating latency and duration. Females mating with a male from the same population produced more eggs, with a lower female bias, over a longer time than females mating with a sibling or with a male from the other population. Mating latency was unaffected by mate relatedness; mating duration was disproportionally long in sibling couples, likely indicating female reluctance to mate and sub-optimal spermatophore transfer. Our study provides a rare example of in- and out-breeding depression in a haplo-diploid arthropod, supporting the optimal outbreeding theory.

Evidence of opposing fitness effects of parental heterozygosity and relatedness in a critically endangered marine turtle?

How individual genetic variability relates to fitness is important in understanding evolution and the processes affecting populations of conservation concern. Heterozygosity-fitness correlations (HFCs) have been widely used to study this link in wild populations, where key parameters that affect both variability and fitness, such as inbreeding, can be difficult to measure. We used estimates of parental heterozygosity and genetic similarity ('relatedness') derived from 32 microsatellite markers to explore the relationship between genetic variability and fitness in a population of the critically endangered hawksbill turtle, Eretmochelys imbricata. We found no effect of maternal MLH (multilocus heterozygosity) on clutch size or egg success rate, and no single-locus effects. However, we found effects of paternal MLH and parental relatedness on egg success rate that interacted in a way that may result in both positive and negative effects of genetic variability. Multicollinearity in these tests was within safe limits, and null simulations suggested that the effect was not an artefact of using paternal genotypes reconstructed from large samples of offspring. Our results could imply a tension between inbreeding and outbreeding depression in this system, which is biologically feasible in turtles: female-biased natal philopatry may elevate inbreeding risk and local adaptation, and both processes may be disrupted by male-biased dispersal. Although this conclusion should be treated with caution due to a lack of significant identity disequilibrium, our study shows the importance of considering both positive and negative effects when assessing how variation in genetic variability affects fitness in wild systems.

Severe outbreeding and inbreeding depression maintain mating system differentiation in Epipactis (Orchidaceae).

In hermaphroditic plants, theory for mating system evolution predicts that populations will evolve to either complete autonomous selfing (AS) or complete outcrossing, depending on the balance between automatic selection favouring self-fertilization and costs resulting from inbreeding depression (ID). Theory also predicts that selection for selfing can occur rapidly and is driven by purging of genetic load and the loss of ID. Therefore, selfing species are predicted to have low levels of ID or even to suffer from outbreeding depression (OD), whereas predominantly outcrossing species are expected to have high levels of ID. To test these predictions, we related the capacity of AS to the magnitude of early-acting inbreeding or OD in both allogamous and autogamous species of the orchid genus Epipactis. For each species, the level of AS was assessed under controlled greenhouse conditions, whereas hand-pollinations were performed to quantify early costs of inbreeding or OD acting at the level of fruit and seed production. In the autogamous species, the capacity of AS was high (> 0.72), whereas in the allogamous species AS was virtually absent (< 0.10). Consistent with our hypothesis, allogamous Epipactis species had significantly higher total ID (average: 0.46) than autogamous species, which showed severe costs of OD (average: -0.45). Overall, our findings indicate that strong early-acting ID represents an important mechanism that contributes to allogamy in Epipactis, whereas OD may maintain selfing in species that have evolved to complete selfing.

Variance and variability, uncovering an underappreciated component of reproductive isolation.

Estimating the fitness of line crosses has been a key element in studies of inbreeding depression, hybridization, and speciation. Fitness values are typically compared using differences in the arithmetic mean of a fitness component between types of crosses. One aspect of fitness that is often overlooked is variance in offspring fitness over time. In the majority of studies, ignoring this aspect of fitness is unavoidable because it is impossible to estimate variance in offspring fitness over long time periods. Here, I describe a method of estimating variance in offspring fitness by substituting spatial variation for temporal variation and provide an empirical example. The method is based on Levene's test of homogeneity of variances. It is implemented by quantifying differences in residual variation among cross types. In a previous study, I performed crosses between populations of the annual plant Diodia teres and quantified hybrid fitness. In this study, another component of isolation and heterosis was revealed when considering variance in offspring fitness. When taking into account variance in offspring fitness using geometric mean fitness as the measure of performance, hybrids between populations from different habitats showed less heterosis than when calculating fitness based on arithmetic mean. This study demonstrates that variance in offspring fitness can be an important aspect of fitness that should be measured more frequently.

Admixture between native and invasive populations may increase invasiveness of Mimulus guttatus.

Self-fertilization and admixture of genotypes from different populations can have major fitness consequences in native species. However, few studies have addressed their potential roles in invasive species. Here, we used plants of Mimulus guttatus from seven native North American, three invasive Scottish and four invasive New Zealand populations to address this. We created seeds from self-fertilization, within-population outcrossing, between-population outcrossing within the same range, and outcrossing between the native and invasive ranges. A greenhouse experiment showed that native and invasive plants of M. guttatus suffered to similar degrees from inbreeding depression, in terms of asexual reproduction and biomass production. After outcrossing with plants from other populations, M. guttatus benefited from heterosis, in terms of asexual and sexual reproduction, and biomass production, particularly when plants from native and invasive populations were crossed. This suggests that, when novel genotypes of M. guttatus from the native North American range will be introduced to the invasive ranges, subsequent outcrossing with M. guttatus plants that are already there might further boost invasiveness of this species.