Moving beyond heritability in the search for coral adaptive potential.

Global environmental change is happening at unprecedented rates. Coral reefs are among the ecosystems most threatened by global change. For wild populations to persist, they must adapt. Knowledge shortfalls about corals' complex ecological and evolutionary dynamics, however, stymie predictions about potential adaptation to future conditions. Here, we review adaptation through the lens of quantitative genetics. We argue that coral adaptation studies can benefit greatly from "wild" quantitative genetic methods, where traits are studied in wild populations undergoing natural selection, genomic relationship matrices can replace breeding experiments, and analyses can be extended to examine genetic constraints among traits. In addition, individuals with advantageous genotypes for anticipated future conditions can be identified. Finally, genomic genotyping supports simultaneous consideration of how genetic diversity is arrayed across geographic and environmental distances, providing greater context for predictions of phenotypic evolution at a metapopulation scale.

The contribution of mutation and selection to multivariate quantitative genetic variance in an outbred population of Drosophila serrata.

Genetic variance is not equal for all multivariate combinations of traits. This inequality, in which some combinations of traits have abundant genetic variation while others have very little, biases the rate and direction of multivariate phenotypic evolution. However, we still understand little about what causes genetic variance to differ among trait combinations. Here, we investigate the relative roles of mutation and selection in determining the genetic variance of multivariate phenotypes. We accumulated mutations in an outbred population of Drosophila serrata and analyzed wing shape and size traits for over 35,000 flies to simultaneously estimate the additive genetic and additive mutational (co)variances. This experimental design allowed us to gain insight into the phenotypic effects of mutation as they arise and come under selection in naturally outbred populations. Multivariate phenotypes associated with more (less) genetic variance were also associated with more (less) mutational variance, suggesting that differences in mutational input contribute to differences in genetic variance. However, mutational correlations between traits were stronger than genetic correlations, and most mutational variance was associated with only one multivariate trait combination, while genetic variance was relatively more equal across multivariate traits. Therefore, selection is implicated in breaking down trait covariance and resulting in a different pattern of genetic variance among multivariate combinations of traits than that predicted by mutation and drift. Overall, while low mutational input might slow evolution of some multivariate phenotypes, stabilizing selection appears to reduce the strength of evolutionary bias introduced by pleiotropic mutation.

Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation.

Adaptation to contrasting environments occurs when advantageous alleles accumulate in each population, but it remains largely unknown whether these same advantageous alleles create genetic incompatibilities that can cause intrinsic reproductive isolation leading to speciation. Identifying alleles that underlie both adaptation and reproductive isolation is further complicated by factors such as dominance and genetic interactions among loci, which can affect both processes differently and obscure potential links between adaptation and speciation. Here, we use a combination of field and glasshouse experiments to explore the connection between adaptation and speciation while accounting for dominance and genetic interactions. We created a hybrid population with equal contributions from four contrasting ecotypes of Senecio lautus (Asteraceae), which produced hybrid genomes both before (F1 hybrid generation) and after (F4 hybrid generation) recombination among the parental ecotypes. In the glasshouse, plants in the second generation (F2 hybrid generation) showed reduced fitness as a loss of fertility. However, fertility was recovered in subsequent generations, suggesting that genetic variation underlying the fitness reduction was lost in subsequent generations. To quantify the effects of losing genetic variation at the F2 generation on the fitness of later generation hybrids, we used a reciprocal transplant to test for fitness differences between parental ecotypes, and F1 and F4 hybrids in all four parental habitats. Compared to the parental ecotypes and F1 hybrids, variance in F4 hybrid fitness was lower, and lowest in habitats that showed stronger native-ecotype advantage, suggesting that stronger natural selection for the native ecotype reduced fitness variation in the F4 hybrids. Fitness trade-offs that were present in the parental ecotypes and F1 hybrids were absent in the F4 hybrid. Together, these results suggest that the genetic variation lost after the F2 generation was likely associated with both adaptation and intrinsic reproductive isolation among ecotypes from contrasting habitats.

MARES, a replicable pipeline and curated reference database for marine eukaryote metabarcoding.

The use of DNA metabarcoding to characterise the biodiversity of environmental and community samples has exploded in recent years. However, taxonomic inferences from these studies are contingent on the quality and completeness of the sequence reference database used to characterise sample species-composition. In response, studies often develop custom reference databases to improve species assignment. The disadvantage of this approach is that it limits the potential for database re-use, and the transferability of inferences across studies. Here, we present the MARine Eukaryote Species (MARES) reference database for use in marine metabarcoding studies, created using a transparent and reproducible pipeline. MARES includes all COI sequences available in GenBank and BOLD for marine taxa, unified into a single taxonomy. Our pipeline facilitates the curation of sequences, synonymization of taxonomic identifiers used by different repositories, and formatting these data for use in taxonomic assignment tools. Overall, MARES provides a benchmark COI reference database for marine eukaryotes, and a standardised pipeline for (re)producing reference databases enabling integration and fair comparison of marine DNA metabarcoding results.

Natural history footage provides new reef fish biodiversity information for a pristine but rarely visited archipelago.

There remain parts of our planet that are seldom visited by humans, let alone scientists. In such locations, crowd-sourced or citizen scientist data can be critical in describing biodiversity and detecting change. Rangitahua, the Kermadec Islands, are 750 km from the nearest human-habitation. Although our knowledge of this near pristine location has increased with recent biodiversity expeditions, we still lack comprehensive understanding of the marine biodiversity surrounding the islands. In 2015, professional underwater videographers were commissioned to produce a nature documentary focused on Rangitahua's reefs. We strategically surveyed the raw documentary video and examined how biodiversity estimates differed from traditional scientific surveys. We uncovered three new fish species records for Rangitahua, extending the known distribution for each species, two of which are also new records for New Zealand waters. Comparison of documentary video footage with scientific survey methods showed that estimates of reef fish species richness from the documentary video were similar to stationary surveys, but lower than non-stationary surveys. Moreover, all survey methods, including documentary video, captured different fish assemblages, reflecting each method's particular bias. Overall, we provide a proof-of-concept for how collaborations between scientists and professional natural historians, such as videographers and photographers, can provide valuable biodiversity information.

Genetic admixture predicts parasite intensity: evidence for increased hybrid performance in Darwin's tree finches.

Hybridization can increase adaptive potential when enhanced genetic diversity or novel genetic combinations confer a fitness advantage, such as in the evolution of anti-parasitic mechanisms. Island systems are especially susceptible to invasive parasites due to the lack of defence mechanisms that usually coevolve in long-standing host-parasite relationships. We test if host genetic admixture affects parasite numbers in a novel host-parasite association on the Galápagos Islands. Specifically, we compare the number of Philornis downsi in nests with offspring sired by Darwin's small tree finch (Camarhynchus parvulus), Darwin's medium tree finch (C. pauper) and hybrids of these two species. The number of P. downsi decreased with an increasing genetic admixture of the attending male, and nests of hybrid males had approximately 50% fewer parasites than C. parvulus nests, and approximately 60% fewer parasites than C. pauper nests. This finding indicates that hybridization in this system could be favoured by selection and reveal a mechanism to combat an invasive parasite.

Environmentally induced development costs underlie fitness tradeoffs.

Local adaptation can lead to genotype-by-environment interactions, which can create fitness tradeoffs in alternative environments, and govern the distribution of biodiversity across geographic landscapes. Exploring the ecological circumstances that promote the evolution of fitness tradeoffs requires identifying how natural selection operates and during which ontogenetic stages natural selection is strongest. When organisms disperse to areas outside their natural range, tradeoffs might emerge when organisms struggle to reach key life history stages, or alternatively, die shortly after reaching life history stages if there are greater risks of mortality associated with costs to developing in novel environments. We used multiple populations from four ecotypes of an Australian native wildflower (Senecio pinnatifolius) in reciprocal transplants to explore how fitness tradeoffs arise across ontogeny. We then assessed whether the survival probability for plants from native and foreign populations was contingent on reaching key developmental stages. We found that fitness tradeoffs emerged as ontogeny progressed when native plants were more successful than foreign plants at reaching seedling establishment and maturity. Native and foreign plants that failed to reach seedling establishment died at the same rate, but plants from foreign populations died quicker than native plants after reaching seedling establishment, and died quicker regardless of whether they reached sexual maturity or not. Development rates were similar for native and foreign populations, but changed depending on the environment. Together, our results suggest that natural selection for environment-specific traits early in life history created tradeoffs between contrasting environments. Plants from foreign populations were either unable to develop to seedling establishment, or they suffered increased mortality as a consequence of reaching seedling establishment. The observation of tradeoffs together with environmentally dependent changes in development rate suggest that foreign environments induce organisms to develop at a rate different from their native habitat, incurring consequences for lifetime fitness and population divergence.

Evolution of Genetic Variance during Adaptive Radiation.

Genetic correlations between traits can concentrate genetic variance into fewer phenotypic dimensions that can bias evolutionary trajectories along the axis of greatest genetic variance and away from optimal phenotypes, constraining the rate of evolution. If genetic correlations limit adaptation, rapid adaptive divergence between multiple contrasting environments may be difficult. However, if natural selection increases the frequency of rare alleles after colonization of new environments, an increase in genetic variance in the direction of selection can accelerate adaptive divergence. Here, we explored adaptive divergence of an Australian native wildflower by examining the alignment between divergence in phenotype mean and divergence in genetic variance among four contrasting ecotypes. We found divergence in mean multivariate phenotype along two major axes represented by different combinations of plant architecture and leaf traits. Ecotypes also showed divergence in the level of genetic variance in individual traits and the multivariate distribution of genetic variance among traits. Divergence in multivariate phenotypic mean aligned with divergence in genetic variance, with much of the divergence in phenotype among ecotypes associated with changes in trait combinations containing substantial levels of genetic variance. Overall, our results suggest that natural selection can alter the distribution of genetic variance underlying phenotypic traits, increasing the amount of genetic variance in the direction of natural selection and potentially facilitating rapid adaptive divergence during an adaptive radiation.

Species identity and depth predict bleaching severity in reef-building corals: shall the deep inherit the reef?

Mass bleaching associated with unusually high sea temperatures represents one of the greatest threats to corals and coral reef ecosystems. Deeper reef areas are hypothesized as potential refugia, but the susceptibility of Scleractinian species over depth has not been quantified. During the most severe bleaching event on record, we found up to 83% of coral cover severely affected on Maldivian reefs at a depth of 3-5 m, but significantly reduced effects at 24-30 m. Analysis of 153 species' responses showed depth, shading and species identity had strong, significant effects on susceptibility. Overall, 73.3% of the shallow-reef assemblage had individuals at a depth of 24-30 m with reduced effects, potentially mitigating local extinction and providing a source of recruits for population recovery. Although susceptibility was phylogenetically constrained, species-level effects caused most lineages to contain some partially resistant species. Many genera showed wide variation between species, including Acropora, previously considered highly susceptible. Extinction risk estimates showed species and lineages of concern and those likely to dominate following repeated events. Our results show that deeper reef areas provide refuge for a large proportion of Scleractinian species during severe bleaching events and that the deepest occurring individuals of each population have the greatest potential to survive and drive reef recovery.

Diversification across a heterogeneous landscape.

Adaptation to contrasting environments across a heterogeneous landscape favors the formation of ecotypes by promoting ecological divergence. Patterns of fitness variation in the field can show whether natural selection drives local adaptation and ecotype formation. However, to demonstrate a link between ecological divergence and speciation, local adaptation must have consequences for reproductive isolation. Using contrasting ecotypes of an Australian wildflower, Senecio lautus in common garden experiments, hybridization experiments, and reciprocal transplants, we assessed how the environment shapes patterns of adaptation and the consequences of adaptive divergence for reproductive isolation. Local adaptation was strong between ecotypes, but weaker between populations of the same ecotype. F1 hybrids exhibited heterosis, but crosses involving one native parent performed better than those with two foreign parents. In a common garden experiment, F2 hybrids exhibited reduced fitness compared to parentals and F1 hybrids, suggesting that few genetic incompatibilities have accumulated between populations adapted to contrasting environments. Our results show how ecological differences across the landscape have created complex patterns of local adaptation and reproductive isolation, suggesting that divergent natural selection has played a fundamental role in the early stages of species diversification.

Genetic Compatibility Underlies Benefits of Mate Choice in an External Fertilizer.

Mate choice is a common feature of sexually reproducing species. In sessile or sedentary external fertilizers, however, direct interactions between reproductive partners are minimal, and instead mate recognition and choice must occur at the level of gametes. It is common for some sperm and egg combinations to have higher fertilization success than others, but it remains unclear whether differences in fertilization reflect gamete-level mate choice (GMC) for paternal quality or parental compatibility. Here, we examine the mechanisms underlying GMC in an externally fertilizing ascidian. A manipulative mate-choice assay confirmed that offspring viability was greater in clutches where we allowed GMC than in clutches where we precluded GMC. A complementary quantitative genetic experiment then revealed that paternal quality effects were generally weaker than parental compatibility effects, particularly for the trait combination underlying the benefits of GMC. Overall, our data suggest that gametes that are more compatible at fertilization produce more viable offspring than gametes that are less compatible at fertilization. Therefore, although the regalia we typically associate with sexual selection are absent in external fertilizers, mechanisms that allow females to bias fertilization in favor of some males over others produce significant fitness benefits in organisms reproducing via the ancestral strategy.

Simultaneous Estimation of Additive and Mutational Genetic Variance in an Outbred Population of Drosophila serrata.

How new mutations contribute to genetic variation is a key question in biology. Although the evolutionary fate of an allele is largely determined by its heterozygous effect, most estimates of mutational variance and mutational effects derive from highly inbred lines, where new mutations are present in homozygous form. In an attempt to overcome this limitation, middle-class neighborhood (MCN) experiments have been used to assess the fitness effect of new mutations in heterozygous form. However, because MCN populations harbor substantial standing genetic variance, estimates of mutational variance have not typically been available from such experiments. Here we employ a modification of the animal model to analyze data from 22 generations of Drosophila serrata bred in an MCN design. Mutational heritability, measured for eight cuticular hydrocarbons, 10 wing-shape traits, and wing size in this outbred genetic background, ranged from 0.0006 to 0.006 (with one exception), a similar range to that reported from studies employing inbred lines. Simultaneously partitioning the additive and mutational variance in the same outbred population allowed us to quantitatively test the ability of mutation-selection balance models to explain the observed levels of additive and mutational genetic variance. The Gaussian allelic approximation and house-of-cards models, which assume real stabilizing selection on single traits, both overestimated the genetic variance maintained at equilibrium, but the house-of-cards model was a closer fit to the data. This analytical approach has the potential to be broadly applied, expanding our understanding of the dynamics of genetic variance in natural populations.

Coral reefs. Limited scope for latitudinal extension of reef corals.

An analysis of present-day global depth distributions of reef-building corals and underlying environmental drivers contradicts a commonly held belief that ocean warming will promote tropical coral expansion into temperate latitudes. Using a global data set of a major group of reef corals, we found that corals were confined to shallower depths at higher latitudes (up to 0.6 meters of predicted shallowing per additional degree of latitude). Latitudinal attenuation of the most important driver of this phenomenon-the dose of photosynthetically available radiation over winter-would severely constrain latitudinal coral range extension in response to ocean warming. Latitudinal gradients in species richness for the group also suggest that higher winter irradiance at depth in low latitudes allowed a deep-water fauna that was not viable at higher latitudes.

The genetic covariance between life cycle stages separated by metamorphosis.

Metamorphosis is common in animals, yet the genetic associations between life cycle stages are poorly understood. Given the radical changes that occur at metamorphosis, selection may differ before and after metamorphosis, and the extent that genetic associations between pre- and post-metamorphic traits constrain evolutionary change is a subject of considerable interest. In some instances, metamorphosis may allow the genetic decoupling of life cycle stages, whereas in others, metamorphosis could allow complementary responses to selection across the life cycle. Using a diallel breeding design, we measured viability at four ontogenetic stages (embryo, larval, juvenile and adult viability), in the ascidian Ciona intestinalis and examined the orientation of additive genetic variation with respect to the metamorphic boundary. We found support for one eigenvector of G: (gobsmax ), which contrasted larval viability against embryo viability and juvenile viability. Target matrix rotation confirmed that while gobsmax shows genetic associations can extend beyond metamorphosis, there is still considerable scope for decoupled phenotypic evolution. Therefore, although genetic associations across metamorphosis could limit that range of phenotypes that are attainable, traits on either side of the metamorphic boundary are capable of some independent evolutionary change in response to the divergent conditions encountered during each life cycle stage.

Mechanisms of biotic resistance across complex life cycles.

Biotic resistance is the ability of communities to inhibit the establishment, spread or impact of novel species. However, the interactions that underlie biotic resistance depend heavily on the contexts in which species interact. Consequently, studies of biotic resistance that consider single processes, patches, species or life-history stages may provide an incomplete picture of the capacity for communities to resist invasion. Many organisms have multiphasic life cycles, where individuals can occupy distinct niches at different stages of the life history. Generally, studies of biotic resistance focus on interactions within a single life-history stage, and interactions at other life-history stages are overlooked. Here, we demonstrate that different mechanisms of biotic resistance occur across the life history and together limit the invasion success of an introduced marine invertebrate (Ciona intestinalis) in Northern California. We tested the role of interactions (competition and predation) with the resident community in limiting the abundance of Ciona through experiments conducted on fertilization, larval survival, settlement, early postsettlement survival, and the survival of juveniles and adults. Under some circumstances, Ciona became abundant in mid-successional stages and showed more rapid growth rates than a morphologically similar native species, Ascidia ceratodes. However, predators reduced Ciona abundance much more than that of Ascidia at several life stages. Furthermore, Ciona appeared to be a weaker competitor at the adult stage. Early life-history interactions with other sessile species at the fertilization, larval and recruit stages had modest to no effects on Ciona abundance. The presence of biotic resistance mechanisms acting at multiple life stages, and potentially under different conditions, suggests that different components of biotic resistance interact to enhance the resident community's resistance to invasion.

Genetic diversity increases population productivity in a sessile marine invertebrate.

Reductions in genetic diversity can have widespread ecological consequences: populations with higher genetic diversity are more stable, productive and resistant to disturbance or disease than populations with lower genetic diversity. These ecological effects of genetic diversity differ from the more familiar evolutionary consequences of depleting genetic diversity, because ecological effects manifest within a single generation. If common, genetic diversity effects have the potential to change the way we view and manage populations, but our understanding of these effects is far from complete, and the role of genetic diversity in sexually reproducing animals remains unclear. Here, we examined the effects of genetic diversity in a sexually reproducing marine invertebrate in the field. We manipulated the genetic diversity of experimental populations and then measured individual survival, growth, and fecundity, as well as the size of offspring produced by individuals in high and low genetic diversity populations. Overall, we found greater genetic diversity increased performance across all metrics, and that complementarity effects drove the increased productivity of our high-diversity populations. Our results show that differences in genetic diversity among populations can have pervasive effects on population productivity within remarkably short periods of time.

Evolutionary optimum for male sexual traits characterized using the multivariate Robertson-Price Identity.

Phenotypes tend to remain relatively constant in natural populations, suggesting a limit to trait evolution. Although stationary phenotypes suggest stabilizing selection, directional selection is more commonly reported. However, selection on phenotypes will have no evolutionary consequence if the traits do not genetically covary with fitness, a covariance known as the Robertson-Price Identity. The nature of this genetic covariance determines if phenotypes will evolve directionally or whether they reside at an evolutionary optimum. Here, we show how a set of traits can be shown to be under net stabilizing selection through an application of the multivariate Robertson-Price Identity. We characterize how a suite of male sexual displays genetically covaries with fitness in a population of Drosophila serrata. Despite strong directional sexual selection on these phenotypes directly and significant genetic variance in them, little genetic covariance was detected with overall fitness. Instead, genetic analysis of trait deviations showed substantial stabilizing selection on the genetic variance of these traits with respect to overall fitness, indicating that they reside at an evolutionary optimum. In the presence of widespread pleiotropy, stabilizing selection on focal traits will arise through the net effects of selection on other, often unmeasured, traits and will tend to be stronger on trait combinations than single traits. Such selection may be difficult to detect in phenotypic analyses if the environmental covariance between the traits and fitness obscures the underlying genetic associations. The genetic analysis of trait deviations provides a way of detecting the missing stabilizing selection inferred by recent metaanalyses.

Does genetic diversity reduce sibling competition?

An enduring hypothesis for the proximal benefits of sex is that recombination increases the genetic variation among offspring and that this genetic variation increases offspring performance. A corollary of this hypothesis is that mothers that mate multiply increase genetic variation within a clutch and gain benefits due to genetic diversity alone. Many studies have demonstrated that multiple mating can increase offspring performance, but most attribute this increase to sexual selection and the role of genetic diversity has received less attention. Here, we used a breeding design to generate populations of full-siblings, half-siblings, and unrelated individuals of the solitary ascidian Ciona intestinalis. Importantly, we preclude the potentially confounding influences of maternal effects and sexual selection. We found that individuals in populations with greater genetic diversity had greater performance (metamorphic success, postmetamorphic survival, and postmetamorphic size) than individuals in populations with lower genetic diversity. Furthermore, we show that by mating with multiple males and thereby increasing genetic variation within a single clutch of offspring, females gain indirect fitness benefits in the absence of mate-choice. Our results show that when siblings are likely to interact, genetic variation among individuals can decrease competition for resources and generate substantial fitness benefits within a single generation.