Pushed waves, trailing edges, and extreme events: Eco-evolutionary dynamics of a geographic range shift in the owl limpet, Lottia gigantea.

As climatic variation re-shapes global biodiversity, understanding eco-evolutionary feedbacks during species range shifts is of increasing importance. Theory on range expansions distinguishes between two different forms: "pulled" and "pushed" waves. Pulled waves occur when the source of the expansion comes from low-density peripheral populations, while pushed waves occur when recruitment to the expanding edge is supplied by high-density populations closer to the species' core. How extreme events shape pushed/pulled wave expansion events, as well as trailing-edge declines/contractions, remains largely unexplored. We examined eco-evolutionary responses of a marine invertebrate (the owl limpet, Lottia gigantea) that increased in abundance during the 2014-2016 marine heatwaves near the poleward edge of its geographic range in the northeastern Pacific. We used whole-genome sequencing from 19 populations across >11 degrees of latitude to characterize genomic variation, gene flow, and demographic histories across the species' range. We estimated present-day dispersal potential and past climatic stability to identify how contemporary and historical seascape features shape genomic characteristics. Consistent with expectations of a pushed wave, we found little genomic differentiation between core and leading-edge populations, and higher genomic diversity at range edges. A large and well-mixed population in the northern edge of the species' range is likely a result of ocean current anomalies increasing larval settlement and high-dispersal potential across biogeographic boundaries. Trailing-edge populations have higher differentiation from core populations, possibly driven by local selection and limited gene flow, as well as high genomic diversity likely as a result of climatic stability during the Last Glacial Maximum. Our findings suggest that extreme events can drive poleward range expansions that carry the adaptive potential of core populations, while also cautioning that trailing-edge extirpations may threaten unique evolutionary variation. This work highlights the importance of understanding how both trailing and leading edges respond to global change and extreme events.

Genomic responses to parallel temperature gradients in the eelgrass Zostera marina in adjacent bays.

The extent of parallel genomic responses to similar selective pressures depends on a complex array of environmental, demographic, and evolutionary forces. Laboratory experiments with replicated selective pressures yield mixed outcomes under controlled conditions and our understanding of genomic parallelism in the wild is limited to a few well-established systems. Here, we examine genomic signals of selection in the eelgrass Zostera marina across temperature gradients in adjacent embayments. Although we find many genomic regions with signals of selection within each bay there is very little overlap in signals of selection at the SNP level, despite most polymorphisms being shared across bays. We do find overlap at the gene level, potentially suggesting multiple mutational pathways to the same phenotype. Using polygenic models we find that some sets of candidate SNPs are able to predict temperature across both bays, suggesting that small but parallel shifts in allele frequencies may be missed by independent genome scans. Together, these results highlight the continuous rather than binary nature of parallel evolution in polygenic traits and the complexity of evolutionary predictability.

Species' attributes predict the relative magnitude of ecological and genetic recovery following mass mortality.

Theoretically, species' characteristics should allow estimation of dispersal potential and, in turn, explain levels of population genetic differentiation. However, a mismatch between traits and genetic patterns is often reported for marine species, and interpreted as evidence that life-history traits do not influence dispersal. Here, we couple ecological and genomic methods to test the hypothesis that species with attributes favouring greater dispersal potential-e.g., longer pelagic duration, higher fecundity and larger population size-have greater realized dispersal overall. We used a natural experiment created by a large-scale and multispecies mortality event which created a "clean slate" on which to study recruitment dynamics, thus simplifying a usually complex problem. We surveyed four species of differing dispersal potential to quantify the abundance and distribution of recruits and to genetically assign these recruits to probable parental sources. Species with higher dispersal potential recolonized a broader extent of the impacted range, did so more quickly and recovered more genetic diversity than species with lower dispersal potential. Moreover, populations of taxa with higher dispersal potential exhibited more immigration (71%-92% of recruits) than taxa with lower dispersal potential (17%-44% of recruits). By linking ecological with genomic perspectives, we demonstrate that a suite of interacting life-history and demographic attributes do influence species' realized dispersal and genetic neighbourhoods. To better understand species' resilience and recovery in this time of global change, integrative eco-evolutionary approaches are needed to more rigorously evaluate the effect of dispersal-linked attributes on realized dispersal and population genetic differentiation.

From the individual to the colony: Marine invertebrates as models to understand levels of biological organization.

The developmental and evolutionary principles of coloniality in marine animals remain largely unexplored. Although many common traits have evolved independently in different groups of colonial animals, questions about their significance for colonial life histories remain unanswered. In 2018 (Nov. 25 - Dec. 8), the inaugural course on the Evolution of Coloniality and Modularity took place at the Center for Marine Biology of the University of São Paulo (CEBIMAR-USP), Brazil. During the intensive two-week graduate-level course, we addressed some of the historical ideas about animal coloniality by focal studies in bryozoans, tunicates, cnidarians, and sponges. We discussed many historical hypotheses and ways to test these using both extant and paleontological data, and we carried direct observations of animal colonies in the different phyla to address questions about coloniality. We covered topics related to multi-level selection theory and studied colonial traits, including modular miniaturization, polymorphism, brooding, and allorecognition. Course participants carried out short research projects using local species of animals to address questions on allorecognition and regeneration in ascidians and sponges, fusion and chimerism in anthoathecate hydrozoans, and evolution of polymorphism in bryozoans. Although many questions remain unanswered, this course served as a foundation to continue to develop a developmental and evolutionary synthesis of clonal and modular development in colonial marine organisms.

The developmental transcriptomes of two sea biscuit species with differing larval types.

BACKGROUND: Larval developmental patterns are extremely varied both between and within phyla, however the genetic mechanisms leading to this diversification are poorly understood. We assembled and compared the developmental transcriptomes for two sea biscuit species (Echinodermata: Echinoidea) with differing patterns of larval development, to provide a resource for investigating the evolution of alternate life cycles. One species (Clypeaster subdepressus) develops via an obligately feeding larva which metamorphoses 3-4 weeks after fertilization; the other (Clypeaster rosaceus) develops via a rare, intermediate larval type-facultative feeding- and can develop through metamorphosis entirely based on egg provisioning in under one week. RESULTS: Overall, the two transcriptomes are highly similar, containing largely orthologous contigs with similar functional annotation. However, we found distinct differences in gene expression patterns between the two species. Larvae from C. rosaceus, the facultative planktotroph, turned genes on at earlier stages and had less differentiation in gene expression between larval stages, whereas, C. subdepressus showed a higher degree of stage-specific gene expression. CONCLUSION: This study is the first genetic analysis of a species with facultatively feeding larvae. Our results are consistent with known developmental differences between the larval types and raise the question of whether earlier onset of developmental genes is a key step in the evolution of a reduced larval period. By publishing a transcriptome for this rare, intermediate, larval type, this study adds developmental breadth to the current genetic resources, which will provide a valuable tool for future research on echinoderm development as well as studies on the evolution of development in general.

Rarity and persistence.

Rarity is a population characteristic that is usually associated with a high risk of extinction. We argue here, however, that chronically rare species (those with low population densities over many generations across their entire ranges) may have individual-level traits that make populations more resistant to extinction. The major obstacle to persistence at low density is successful fertilisation (union between egg and sperm), and chronically rare species are more likely to survive when (1) fertilisation occurs inside or close to an adult, (2) mate choice involves long-distance signals, (3) adults or their surrogate gamete dispersers are highly mobile, or (4) the two sexes are combined in a single individual. In contrast, external fertilisation and wind- or water-driven passive dispersal of gametes, or sluggish or sedentary adult life habits in the absence of gamete vectors, appear to be incompatible with sustained rarity. We suggest that the documented increase in frequency of these traits among marine genera over geological time could explain observed secular decreases in rates of background extinction. Unanswered questions remain about how common chronic rarity actually is, which traits are consistently associated with chronic rarity, and how chronically rare species are distributed among taxa, and among the world's ecosystems and regions.

The sea as deathtrap: comment on a paper by miller and wiens.

Miller & Wiens (2017) claim that low marine as compared with terrestrial diversity results from more frequent extinctions and insufficient time for diversification in marine clades. Their data on marine amniotes are unrepresentative of marine diversity, their analysis of clade dynamics is flawed, and they ignore previously proposed explanations for the diversity difference.

Multiple dimensions of intraspecific diversity affect biomass of eelgrass and its associated community.

Genetic diversity within key species can play an important role in the functioning of entire communities. However, the extent to which different dimensions of diversity (e.g., the number of genotypes vs. the extent of genetic differentiation among those genotypes) best predicts functioning is unknown and may yield clues into the different mechanisms underlying diversity effects. We explicitly test the relative influence of genotypic richness and genetic relatedness on eelgrass productivity, biomass, and the diversity of associated invertebrate grazers in a factorial field experiment using the seagrass species, Zostera marina (eelgrass). Genotypic richness had the strongest effect on eelgrass biomass accumulation, such that plots with more genotypes at the end of the experiment attained a higher biomass. Genotypic diversity (richness + evenness) was a stronger predictor of biomass than richness alone, and both genotype richness and diversity were positively correlated with trait diversity. The relatedness of genotypes in a plot reduced eelgrass biomass independently of richness. Plots containing eelgrass with greater trait diversity also had a higher abundance of invertebrate grazers, while the diversity and relatedness of eelgrass genotypes had little effect on invertebrate abundance or richness. Our work extends previous findings by explicitly relating genotypic diversity to trait diversity, thus mechanistically connecting genotypic diversity to plot-level yields. We also show that other dimensions of diversity, namely relatedness, influence eelgrass performance independent of trait differentiation. Ultimately, richness and relatedness captured fundamentally different components of intraspecific variation and should be treated as complementary rather than competing dimensions of biodiversity affecting ecosystem functioning.

In memoriam: Richard G. Harrison - his life and legacy.

Richard G. Harrison passed away unexpectedly on April 12th, 2016. In this memoriam we pay tribute to the life and legacy of an extraordinary scientist, mentor, friend, husband, and father.

Trade-offs, geography, and limits to thermal adaptation in a tide pool copepod.

Antagonistic correlations among traits may slow the rate of adaptation to a changing environment. The tide pool copepod Tigriopus californicus is locally adapted to temperature, but within populations, the response to selection for increased heat tolerance plateaus rapidly, suggesting either limited variation within populations or costs of increased tolerance. To measure possible costs of thermal tolerance, we selected for increased upper lethal limits for 10 generations in 22 lines of T. californicus from six populations. Then, for each line, we measured six fitness-related traits. Selected lines showed an overall increase in male and female body sizes, fecundity, and starvation resistance, suggesting a small benefit from (rather than costs of) increased tolerance. The effect of selection on correlated traits also varied significantly by population for five traits, indicating that the genetic basis for the selection response differed among populations. Our results suggest that adaptation was limited by the presence of variation within isolated populations rather than by costs of increased tolerance.

Genetic relatedness influences plant biomass accumulation in eelgrass (Zostera marina).

In multispecies assemblages, phylogenetic relatedness often predicts total community biomass. In assemblages dominated by a single species, increasing the number of genotypes increases total production, but the role of genetic relatedness is unknown. We used data from three published experiments and a field survey of eelgrass (Zostera marina), a habitat-forming marine angiosperm, to examine the strength and direction of the relationship between genetic relatedness and plant biomass. The genetic relatedness of an assemblage strongly predicted its biomass, more so than the number of genotypes. However, contrary to the pattern observed in multispecies assemblages, maximum biomass occurred in assemblages of more closely related individuals. The mechanisms underlying this pattern remain unclear; however, our data support a role for both trait differentiation and cooperation among kin. Many habitat-forming species interact intensely with conspecifics of varying relatedness; thus, genetic relatedness could influence the functioning of ecosystems dominated by such species.

Kinship and the evolution of social behaviours in the sea.

Until recently, little attention has been paid to the existence of kin structure in the sea, despite the fact that many marine organisms are sessile or sedentary. This lack of attention to kin structure, and its impacts on social evolution, historically stems from the pervasive assumption that the dispersal of gametes and larvae is almost always sufficient to prevent any persistent associations of closely related offspring or adults. However, growing evidence, both theoretical and empirical, casts doubt on the generality of this assumption, not only in species with limited dispersal, but also in species with long dispersive phases. Moreover, many marine organisms either internally brood their progeny or package them in nurseries, both of which provide ample opportunities for kinship to influence the nature and outcomes of social interactions among family members. As the evidence for kin structure within marine populations mounts, it follows that kin selection may play a far greater role in the evolution of both behaviours and life histories of marine organisms than is presently appreciated.

Shallow gene pools in the high intertidal: extreme loss of genetic diversity in viviparous sea stars (Parvulastra).

We document an extreme example of reproductive trait evolution that affects population genetic structure in sister species of Parvulastra cushion stars from Australia. Self-fertilization by hermaphroditic adults and brood protection of benthic larvae causes strong inbreeding and range-wide genetic poverty. Most samples were fixed for a single allele at nearly all nuclear loci; heterozygotes were extremely rare (0.18%); mitochondrial DNA sequences were more variable, but few populations shared haplotypes in common. Isolation-with-migration models suggest that these patterns are caused by population bottlenecks (relative to ancestral population size) and low gene flow. Loss of genetic diversity and low potential for dispersal between high-intertidal habitats may have dire consequences for extinction risk and potential for future adaptive evolution in response to climate and other selective agents.

Exclusive male care despite extreme female promiscuity and low paternity in a marine snail.

Males exhibit striking variation in the degree to which they invest in offspring, from merely provisioning females with sperm, to providing exclusive post-zygotic care. Paternity assurance is often invoked to explain this variation: the greater a male's confidence of paternity, the more he should be willing to provide care. Here, we report a striking exception to expectations based on paternity assurance: despite high levels of female promiscuity, males of a marine snail provide exclusive, and costly, care of offspring. Remarkably, genetic paternity analyses reveal cuckoldry in all broods, with fewer than 25% of offspring being sired by the caring male, although caring males sired proportionally more offspring in a given clutch than any other fathers did individually. This system presents the most extreme example of the coexistence of high levels of female promiscuity, low paternity, and costly male care, and emphasises the still unresolved roles of natural and sexual selection in the evolution of male parental care.

Limited potential for adaptation to climate change in a broadly distributed marine crustacean.

The extent to which acclimation and genetic adaptation might buffer natural populations against climate change is largely unknown. Most models predicting biological responses to environmental change assume that species' climatic envelopes are homogeneous both in space and time. Although recent discussions have questioned this assumption, few empirical studies have characterized intraspecific patterns of genetic variation in traits directly related to environmental tolerance limits. We test the extent of such variation in the broadly distributed tidepool copepod Tigriopus californicus using laboratory rearing and selection experiments to quantify thermal tolerance and scope for adaptation in eight populations spanning more than 17° of latitude. Tigriopus californicus exhibit striking local adaptation to temperature, with less than 1 per cent of the total quantitative variance for thermal tolerance partitioned within populations. Moreover, heat-tolerant phenotypes observed in low-latitude populations cannot be achieved in high-latitude populations, either through acclimation or 10 generations of strong selection. Finally, in four populations there was no increase in thermal tolerance between generations 5 and 10 of selection, suggesting that standing variation had already been depleted. Thus, plasticity and adaptation appear to have limited capacity to buffer these isolated populations against further increases in temperature. Our results suggest that models assuming a uniform climatic envelope may greatly underestimate extinction risk in species with strong local adaptation.

Extraordinarily rapid life-history divergence between Cryptasterina sea star species.

Life history plays a critical role in governing microevolutionary processes such as gene flow and adaptation, as well as macroevolutionary processes such speciation. Here, we use multilocus phylogeographic analyses to examine a speciation event involving spectacular life-history differences between sister species of sea stars. Cryptasterina hystera has evolved a suite of derived life-history traits (including internal self-fertilization and brood protection) that differ from its sister species Cryptasterina pentagona, a gonochoric broadcast spawner. We show that these species have only been reproductively isolated for approximately 6000 years (95% highest posterior density of 905-22 628), and that this life-history change may be responsible for dramatic genetic consequences, including low nucleotide diversity, zero heterozygosity and no gene flow. The rapid divergence of these species rules out some mechanisms of isolation such as adaptation to microhabitats in sympatry, or slow divergence by genetic drift during prolonged isolation. We hypothesize that the large phenotypic differences between species relative to the short divergence time suggests that the life-history differences observed may be direct responses to disruptive selection between populations. We speculate that local environmental or demographic differences at the southern range margin are possible mechanisms of selection driving one of the fastest known marine speciation events.

Love the one you're with: proximity determines paternity success in the barnacle Tetraclita rubescens.

A species' mating system sets limits on the strength of sexual selection. Sexual selection is widespread in dioecious species, but is less well documented in hermaphrodites, and may be less important. We used four highly polymorphic microsatellite markers to assign paternity to broods of the hermaphroditic eastern Pacific volcano barnacle Tetraclita rubescens. These data were used to describe the species' mating system and to examine factors affecting male reproductive success. Tetraclita can sire broods over distances of 11.2 cm, but proximity to the sperm recipient had a highly significant effect on the probability of siring success. There was no effect of body size or the mass of male reproductive tissues on siring success. Broods showed relatively low frequencies of multiple paternity; even at high densities, 75% of broods had only one father. High frequencies of single-paternity broods imply either that this species does not compete via sperm displacement, or that sperm displacement is extremely effective, potentially explaining the lack of a positive relationship between male investment and paternity. In addition, there was low variance in siring success among individuals, suggesting a lack of strong sexual selection on male traits. Low variance among sires and the strong effect of proximity are probably driven by the unusual biology of a sessile copulating species.

Constraints on the use of lifespan-shortening Wolbachia to control dengue fever.

Dengue fever, a viral disease spread by the mosquito Aedes aegypti, affects 50-100 million people a year in many tropical countries. Because the virus must incubate within mosquito hosts for two weeks before being able to transmit the infection, shortening the lifespan of mosquitoes may curtail dengue transmission. We developed a continuous time reaction-diffusion model of the spatial spread of Wolbachia through a population of A. aegypti. This model incorporates the lifespan-shortening effects of Wolbachia on infected A. aegypti and the fitness advantage to infected females due to cytoplasmic incompatibility (CI). We found that local establishment of the Wolbachia infection can occur if the fitness advantage due to CI exceeds the fitness reduction due to lifespan-shortening effects, in accordance with earlier results concerning fecundity reduction. However, spatial spread is possible only if the fitness advantage due to CI is twice as great as the fitness reduction due to lifespan shortening effects. Moreover, lifespan-shortening and fecundity-reduction can have different effects on the speed of wave-retreat. Using data from the literature, we estimated all demographic parameters for infected and uninfected mosquitoes and computed the velocities of spread of infection. Our most optimistic estimates suggest that the spatial spread of lifespan-shortening Wolbachia may be so slow that efficient spatial spread would require a prohibitively large number of point releases. However, as these estimates of demographic parameters may not accurately reflect natural conditions, further research is necessary to corroborate these predictions.

Caterpillars did not evolve from onychophorans by hybridogenesis.

The evolution and loss of distinctive larval forms in animal life cycles have produced complex patterns of similarity and difference among life-history stages and major animal lineages. One example of this similarity is the morphological forms of Onychophora (velvet worms) and the caterpillar-like larvae of some insects. Williamson [(2009) Proc Natl Acad Sci USA 106:15786-15790] has made the astonishing and unfounded claim that the ancestors of the velvet worms directly gave rise to insect caterpillars via hybridization and that evidence of this ancient "larval transfer" could be found in comparisons among the genomes of extant onychophorans, insects with larvae, and insects without larvae. Williamson has made a series of predictions arising from his hypothesis and urged genomicists to test them. Here, we use data already in the literature to show these predictions to be false. Hybridogenesis between distantly related animals does not explain patterns of morphological and life-history evolution in general, and the genes and genomes of animals provide strong evidence against hybridization or larval transfer between a velvet worm and an insect in particular.

Post-glacial redistribution and shifts in productivity of giant kelp forests.

Quaternary glacial-interglacial cycles create lasting biogeographic, demographic and genetic effects on ecosystems, yet the ecological effects of ice ages on benthic marine communities are unknown. We analysed long-term datasets to develop a niche-based model of southern Californian giant kelp (Macrocystis pyrifera) forest distribution as a function of oceanography and geomorphology, and synthesized palaeo-oceanographic records to show that late Quaternary climate change probably drove high millennial variability in the distribution and productivity of this foundation species. Our predictions suggest that kelp forest biomass increased up to threefold from the glacial maximum to the mid-Holocene, then rapidly declined by 40-70 per cent to present levels. The peak in kelp forest productivity would have coincided with the earliest coastal archaeological sites in the New World. Similar late Quaternary changes in kelp forest distribution and productivity probably occurred in coastal upwelling systems along active continental margins worldwide, which would have resulted in complex shifts in the relative productivity of terrestrial and marine components of coastal ecosystems.