Polymorphism and the Red Queen: the selective maintenance of allelic variation in a deteriorating environment.

Although allelic variation is ubiquitous in natural populations, our theoretical models are poor at predicting the existence and properties of these observed polymorphisms. In this study, inspired by Van Valen's Red Queen hypothesis, we modeled the effect of viability selection in a deteriorating environment on the properties of allelic variation in populations subject to recurrent mutation. In Monte Carlo simulations, we found that levels of polymorphism consistently built up over time. We censused the simulated populations after 10,000 generations of mutation and selection, revealing that, compared with models assuming a constant environment, the mean number of alleles was greater, as was the range of allele numbers. These results were qualitatively robust to the addition of genetic drift and to the relaxation of the assumption that the viabilities of phenogenotypes containing a new mutation are independent of each other (i.e. incorporating a model of generalized dominance). The broad range of allele numbers realized in the simulated populations-from monomorphisms to highly polymorphic populations-more closely corresponds to the observed range from numerous surveys of natural populations than previously found in theoretical studies. This match suggests that, contrary to the views of some writers, selection may actively maintain genetic variation in natural populations, particularly if the selective environment is gradually becoming harsher. Our simulations also generated many populations with heterozygote advantage, a mismatch with real data that implies that this selective property must arise extremely rarely in natural populations.

Boring bryozoans: an investigation into the endolithic bryozoan family Penetrantiidae.

An endolithic lifestyle in mineralized substrates has evolved multiple times in various phyla including Bryozoa. The family Penetrantiidae includes one genus with ten extant and two fossil species. They predominantly colonize the shells of molluscs and establish colonies by chemical dissolution of calcium carbonate. Based on several morphological characters, they were described to be either cheilostome or ctenostome bryozoans. For more than 40 years, neither the characters of species identity and systematics nor the problem of their phylogeny was approached. Consequently, the aim of this study is to reevaluate species identities and the systematic position of the genus Penetrantia by analyzing at least six different species from eight regions with the aid of modern methods such as confocal laser scanning microscopy and 3D-reconstruction techniques. This study demonstrates that the musculature associated with the operculum and brood chamber shows significant differences from the cheilostome counterparts and seems to have evolved independently. Together with the presence of other ctenostome-like features such as true polymorphic stolons and uncalcified body wall, this finding supports a ctenostome affinity. Operculum morphology reveals many new species-specific characters, which, together with information about gonozooid morphology, tentacle number, and zooid size ranges, will enhance species identification. It also revealed a probable new species in Japan as well as potential cryptic species in France and New Zealand. In addition, this study increases the known distribution range of the family and its substrate diversity. Altogether, the new information collated here provides the basis for future work on a neglected taxon. Supplementary Information: The online version contains supplementary material available at 10.1007/s13127-023-00612-z.

The swan genome and transcriptome, it is not all black and white.

BACKGROUND: The Australian black swan (Cygnus atratus) is an iconic species with contrasting plumage to that of the closely related northern hemisphere white swans. The relative geographic isolation of the black swan may have resulted in a limited immune repertoire and increased susceptibility to infectious diseases, notably infectious diseases from which Australia has been largely shielded. Unlike mallard ducks and the mute swan (Cygnus olor), the black swan is extremely sensitive to highly pathogenic avian influenza. Understanding this susceptibility has been impaired by the absence of any available swan genome and transcriptome information. RESULTS: Here, we generate the first chromosome-length black and mute swan genomes annotated with transcriptome data, all using long-read based pipelines generated for vertebrate species. We use these genomes and transcriptomes to show that unlike other wild waterfowl, black swans lack an expanded immune gene repertoire, lack a key viral pattern-recognition receptor in endothelial cells and mount a poorly controlled inflammatory response to highly pathogenic avian influenza. We also implicate genetic differences in SLC45A2 gene in the iconic plumage of the black swan. CONCLUSION: Together, these data suggest that the immune system of the black swan is such that should any avian viral infection become established in its native habitat, the black swan would be in a significant peril.

Application of palaeogenetic techniques to historic mollusc shells reveals phylogeographic structure in a New Zealand abalone.

Natural history collections worldwide contain a plethora of mollusc shells. Recent studies have detailed the sequencing of DNA extracted from shells up to thousands of years old and from various taphonomic and preservational contexts. However, previous approaches have largely addressed methodological rather than evolutionary research questions. Here, we report the generation of DNA sequence data from mollusc shells using such techniques, applied to Haliotis virginea Gmelin, 1791, a New Zealand abalone, in which morphological variation has led to the recognition of several forms and subspecies. We successfully recovered near-complete mitogenomes from 22 specimens including 12 dry-preserved shells up to 60 years old. We used a combination of palaeogenetic techniques that have not previously been applied to shell, including DNA extraction optimized for ultra-short fragments and hybridization-capture of single-stranded DNA libraries. Phylogenetic analyses revealed three major, well-supported clades comprising samples from: (1) The Three Kings Islands; (2) the Auckland, Chatham and Antipodes Islands; and (3) mainland New Zealand and Campbell Island. This phylogeographic structure does not correspond to the currently recognized forms. Critically, our nonreliance on freshly collected or ethanol-preserved samples enabled inclusion of topotypes of all recognized subspecies as well as additional difficult-to-sample populations. Broader application of these comparatively cost-effective and reliable methods to modern, historical, archaeological and palaeontological shell samples has the potential to revolutionize invertebrate genetic research.

Epigenetic induction may speed up or slow down speciation with gene flow.

Speciation is less likely to occur when there is gene flow between nascent species. Natural selection can oppose gene flow and promote speciation if there is variation in ecological conditions among the nascent species' locations. Previous theory on ecological speciation with gene flow has focused primarily on the role of genetic variation in ecological traits, largely neglecting the role of nongenetic inheritance or transgenerational plasticity. Here, we build and analyze models incorporating both genetic and epigenetic inheritance, the latter representing a form of nongenetic inheritance. We investigate the rate of speciation for a population that inhabits two patches connected by migration, and find that adaptively biased epigenetic induction can speed up or slow down speciation, depending on the form of the map from genotype and epigenotype to phenotype. While adaptively relevant epigenetic variation can speed up speciation by reducing the fitness of migrants and hybrids, it can also slow down speciation. This latter effect occurs when the epialleles are able to achieve adaptation faster than the genetic alleles, thereby weakening selection on the latter.

A model of optimal timing for a predictive adaptive response.

Predictive adaptive responses (PARs) are a form of developmental plasticity in which the developmental response to an environmental cue experienced early in life is delayed and yet, at the same time, the induced phenotype anticipates (i.e., is completely developed before) exposure to the eventual environmental state predicted by the cue, in which the phenotype is adaptive. We model this sequence of events to discover, under various assumptions concerning the cost of development, what lengths of delay, developmental time, and anticipation are optimal. We find that in many scenarios modeled, development of the induced phenotype should be completed at the exact same time that the environmental exposure relevant to the induced phenotype begins: that is, in contrast to our observed cases of PARs, there should be no anticipation. Moreover, unless slow development is costly, development should commence immediately after the cue: there should be no delay. Thus, PARs, which normally have non-zero delays and/or anticipation, are highly unusual. Importantly, the exceptions to these predictions of zero delays and anticipation occurred when developmental time was fixed and delaying development was increasingly costly. We suggest, therefore, that PARs will only evolve under three kinds of circumstances: (i) there are strong timing constraints on the cue and the environmental status, (ii) delaying development is costly, and development time is either fixed or slow development is costly, or (iii) when the period between the cue and the eventual environmental change is variable and the cost of not completing development before the change is high. These predictions are empirically testable.

Complete distribution of the genus Laevilitorina (Littorinimorpha, Littorinidae) in the Southern Hemisphere: remarks and natural history.

Littorinid snails are present in most coastal areas globally, playing a significant role in the ecology of intertidal communities. Laevilitorina is a marine gastropod genus distributed exclusively in the Southern Hemisphere, with 21 species reported from South America, the sub-Antarctic islands, Antarctica, New Zealand, Australia and Tasmania. Here, an updated database of 21 species generated from a combination of sources is presented: 1) new field sampling data; 2) published records; 3) the Global Biodiversity Information Facility (GBIF) and The Atlas of Living Australia (ALA), to provide a comprehensive description of the known geographic distribution of the genus and detailed occurrences for each of the 21 species. The database includes 813 records (occurrences), 53 from field sampling, 174 from the literature, 128 from GBIF, and 458 from ALA. West Antarctica had the highest species richness (8 species), followed by sub-Antarctic islands of New Zealand (4 species) and the south-east shelf of Australia (4 species). The provinces of Magellan, New Zealand South Island, and sub-Antarctic Islands of the Indian Ocean include two species each. This study specifically highlights reports of L.pygmaea and L.venusta, species that have been almost unrecorded since their description. Recent advances in molecular studies of L.caliginosa showed that this species does not correspond to a widely distributed taxon, but to multiple divergent lineages distributed throughout the Southern Ocean. Ongoing molecular and taxonomic studies are necessary for a better understanding of the diversity and biogeography of this genus.

Avoiding extinction under nonlinear environmental change: models of evolutionary rescue with plasticity.

Rapid environmental changes are putting numerous species at risk of extinction. For migration-limited species, persistence depends on either phenotypic plasticity or evolutionary adaptation (evolutionary rescue). Current theory on evolutionary rescue typically assumes linear environmental change. Yet accelerating environmental change may pose a bigger threat. Here, we present a model of a species encountering an environment with accelerating or decelerating change, to which it can adapt through evolution or phenotypic plasticity (within-generational or transgenerational). We show that unless either form of plasticity is sufficiently strong or adaptive genetic variation is sufficiently plentiful, accelerating or decelerating environmental change increases extinction risk compared to linear environmental change for the same mean rate of environmental change.

Graph-structured populations and the Hill-Robertson effect.

The Hill-Robertson effect describes how, in a finite panmictic diploid population, selection at one diallelic locus reduces the fixation probability of a selectively favoured allele at a second, linked diallelic locus. Here we investigate the influence of population structure on the Hill-Robertson effect in a population of size N. We model population structure as a network by assuming that individuals occupy nodes on a graph connected by edges that link members who can reproduce with each other. Three regular networks (fully connected, ring and torus), two forms of scale-free network and a star are examined. We find that (i) the effect of population structure on the probability of fixation of the favourable allele is invariant for regular structures, but on some scale-free networks and a star, this probability is greatly reduced; (ii) compared to a panmictic population, the mean time to fixation of the favoured allele is much greater on a ring, torus and linear scale-free network, but much less on power-2 scale-free and star networks; (iii) the likelihood with which each of the four possible haplotypes eventually fix is similar across regular networks, but scale-free populations and the star are consistently less likely and much faster to fix the optimal haplotype; (iv) increasing recombination increases the likelihood of fixing the favoured haplotype across all structures, whereas the time to fixation of that haplotype usually increased, and (v) star-like structures were overwhelmingly likely to fix the least fit haplotype and did so significantly more rapidly than other populations. Last, we find that small (N < 64) panmictic populations do not exhibit the scaling property expected from Hill & Robertson (1966 Genet. Res. 8, 269-294. (doi:10.1017/S0016672300010156)).

Catalogue of New Zealand land, freshwater and estuarine molluscan taxa named by Frederick Wollaston Hutton between 1879 and 1904.

Details are provided on 16 land snail genera, eight freshwater molluscan species, one estuarine species, 47 land snail species and varieties from New Zealand, and a further three land snail species putatively from New Zealand, which were described by Frederick Wollaston Hutton between 1879 and 1904. Original primary type material of 54 species was located during the present study. Lectotypes are designated for: Amphidoxa cornea Hutton, 1882, Amphidoxa jacquenetta Hutton, 1883, Amphidoxa perdita Hutton, 1883, Charopa cassandra Hutton, 1883, Cyclotus charmian Hutton, 1883, Fruticicola adriana Hutton, 1883, Gerontia cordelia Hutton, 1883, Gerontia pantherina Hutton, 1882, Microphysa pumila Hutton, 1882, Patula jessica Hutton, 1883, Patula lucetta Hutton, 1884, Patula sylvia Hutton, 1883, Patula tapirina Hutton, 1882, Pfeifferia cressida Hutton, 1883, Phrixgnathus celia Hutton, 1883, Phrixgnathus haasti Hutton, 1883, Phrixgnathus marginatus Hutton, 1882, Phrixgnathus phrynia Hutton, 1883, Rhytida australis Hutton, 1882, Strobila leiodon Hutton, 1882, Thalassia propinqua Hutton, 1882, Therasia thaisa Hutton, 1883, Therasia valeria Hutton, 1883 and Zonites helmsii Hutton, 1882. A neotype is designated for Rhytida citrina Hutton, 1882. Primary type material of the following taxa is figured herein for the first time: Amphidoxa lavinia Hutton, 1883, Cyclotus charmian Hutton, 1883, Fruticicola adriana Hutton, 1883, Leptopoma pannosa Hutton, 1882, Patula lucetta Hutton, 1884, Patula sylvia Hutton, 1883, Patula tapirina Hutton, 1882, Phacussa helmsi var. maculata Hutton, 1884, Phrixgnathus ariel Hutton, 1883, Phrixgnathus celia Hutton, 1883, Rhytida australis Hutton, 1882, Rissoa vana Hutton, 1873, Testacella vagans Hutton, 1882, Trochomorpha hermia Hutton, 1883 and Zonites helmsii Hutton, 1882. New taxonomic combinations introduced herein include Phacussa lucetta (Hutton, 1884) and Therasia propinqua (Hutton, 1882). Amphidoxa lavinia Hutton, 1883, Charopa cassandra Hutton, 1883, Patula timandra Hutton, 1883 and Trochomorpha hermia Hutton, 1883 are treated as junior synonyms of Tasmaphena sinclairii (Pfeiffer, 1846), Phacussa fulminata (Hutton, 1882), Fectola infecta (Reeve, 1852) and Advena campbellii (Gray, 1834), respectively.

Species-level biodiversity assessment using marine environmental DNA metabarcoding requires protocol optimization and standardization.

DNA extraction from environmental samples (environmental DNA; eDNA) for metabarcoding-based biodiversity studies is gaining popularity as a noninvasive, time-efficient, and cost-effective monitoring tool. The potential benefits are promising for marine conservation, as the marine biome is frequently under-surveyed due to its inaccessibility and the consequent high costs involved. With increasing numbers of eDNA-related publications have come a wide array of capture and extraction methods. Without visual species confirmation, inconsistent use of laboratory protocols hinders comparability between studies because the efficiency of target DNA isolation may vary. We determined an optimal protocol (capture and extraction) for marine eDNA research based on total DNA yield measurements by comparing commonly employed methods of seawater filtering and DNA isolation. We compared metabarcoding results of both targeted (small taxonomic group with species-level assignment) and universal (broad taxonomic group with genus/family-level assignment) approaches obtained from replicates treated with the optimal and a low-performance capture and extraction protocol to determine the impact of protocol choice and DNA yield on biodiversity detection. Filtration through cellulose-nitrate membranes and extraction with Qiagen's DNeasy Blood & Tissue Kit outperformed other combinations of capture and extraction methods, showing a ninefold improvement in DNA yield over the poorest performing methods. Use of optimized protocols resulted in a significant increase in OTU and species richness for targeted metabarcoding assays. However, changing protocols made little difference to the OTU and taxon richness obtained using universal metabarcoding assays. Our results demonstrate an increased risk of false-negative species detection for targeted eDNA approaches when protocols with poor DNA isolation efficacy are employed. Appropriate optimization is therefore essential for eDNA monitoring to remain a powerful, efficient, and relatively cheap method for biodiversity assessments. For seawater, we advocate filtration through cellulose-nitrate membranes and extraction with Qiagen's DNeasy Blood & Tissue Kit or phenol-chloroform-isoamyl for successful implementation of eDNA multi-marker metabarcoding surveys.

The phylogenetic placement of the enigmatic Indian Cormorant, Phalacrocorax fuscicollis (Phalacrocoracidae).

The Indian Cormorant (Phalacrocorax fuscicollis) is a common avian piscivore that occurs throughout the Indian subcontinent and east to southern Vietnam. Its evolutionary relationships, however, have remained obscure, largely because of a lack of material available for either osteological or genetic analysis. Here we show using DNA-sequence data from both nuclear and mitochondrial genes that this species is sister to the allopatric Little Black Cormorant (P. sulcirostris), which occurs from Java in the west through southern Indonesia and New Guinea to Australia and New Zealand in the south. We estimate this split to have happened 2.5-3.2 million years ago, during the late Pliocene. We also report on genetic variation within the mitochondrial control region, which suggests that this part of the genome may be useful in investigating if there is genetic structure across the geographical range of the Indian Cormorant.

Environmental DNA (eDNA) metabarcoding reveals strong discrimination among diverse marine habitats connected by water movement.

While in recent years environmental DNA (eDNA) metabarcoding surveys have shown great promise as an alternative monitoring method, the integration into existing marine monitoring programs may be confounded by the dispersal of the eDNA signal. Currents and tidal influences could transport eDNA over great distances, inducing false-positive species detection, leading to inaccurate biodiversity assessments and, ultimately, mismanagement of marine environments. In this study, we determined the ability of eDNA metabarcoding surveys to distinguish localized signals obtained from four marine habitats within a small spatial scale (<5 km) subject to significant tidal and along-shore water flow. Our eDNA metabarcoding survey detected 86 genera, within 77 families and across 11 phyla using three established metabarcoding assays targeting fish (16S rRNA gene), crustacean (16S rRNA gene) and eukaryotic (cytochrome oxidase subunit 1) diversity. Ordination and cluster analyses for both taxonomic and OTU data sets show distinct eDNA signals between the sampled habitats, suggesting dispersal of eDNA among habitats was limited. Individual taxa with strong habitat preferences displayed localized eDNA signals in accordance with their respective habitat, whereas taxa known to be less habitat-specific generated more ubiquitous signals. Our data add to evidence that eDNA metabarcoding surveys in marine environments detect a broad range of taxa that are spatially discrete. Our work also highlights that refinement of assay choice is essential to realize the full potential of eDNA metabarcoding surveys in marine biodiversity monitoring programs.

The evolution of epigenetically mediated adaptive transgenerational plasticity in a subdivided population.

Transgenerational plasticity (TGP) occurs when offspring exhibit plasticity in traits induced by the environments experienced by their parents, and represents a nongenetic mechanism of inheritance. Evidence that traits can be transmitted to future generations by means other than genetic inheritance has caused a surge of interest in epigenetic inheritance, but evidence for epigenetic modifications being both adaptive and heritable remains scarce. What features would make a species most prone to evolve a system of epigenetically mediated adaptive TGP? Here, we use population-genetic models modified to include epigenetic induction and inheritance to investigate if and when epigenetically mediated adaptive TGP would be expected to evolve for a population subdivided between two habitats connected by migration. We show that differences in the direction of selection between the two habitats drives the evolution of epigenetically mediated adaptive TGP. With low migration, the strength of indirect selection in favor of epigenetically mediated adaptive TGP increases with migration rate. Yet, with higher migration, the opposite trend is observed. We predict that species subdivided between habitats that differ in the direction of selection with moderate migration rates between the habitats would be most likely to evolve epigenetically mediated adaptive TGP if costs of producing such systems are not too high.

Speciation, range contraction and extinction in the endemic New Zealand King Shag complex.

New Zealand's endemic King Shag (Leucocarbo carunculatus) has occupied only a narrow portion of the northeastern South Island for at least the past 240years. However, pre-human Holocene fossil and archaeological remains have suggested a far more widespread distribution of the three Leucocarbo species (King, Otago, Foveaux) on mainland New Zealand at the time of Polynesian settlement in the late 13th Century CE. We use modern and ancient DNA, and morphometric and osteological analyses, of modern King Shags and Holocene fossil Leucocarbo remains to assess the pre-human distribution and taxonomic status of the King Shag on mainland New Zealand, and the resultant conservation implications. Our analyses show that the King Shag was formerly widespread around southern coasts of the North Island and the northern parts of the South Island but experienced population and lineage extinctions, and range contraction, probably after Polynesian arrival. This history parallels range contractions of other New Zealand seabirds. Conservation management of the King Shag should take into account this species narrow distribution and probable reduced genetic diversity. Moreover, combined genetic, morphometric and osteological analyses of prehistoric material from mainland New Zealand suggest that the now extinct northern New Zealand Leucocarbo populations comprised a unique lineage. Although these distinctive populations were previously assigned to the King Shag (based on morphological similarities and geographic proximity to modern Leucocarbo populations), we herein describe them as a new species, the Kohatu Shag (Leucocarbo septentrionalis). The extinction of this species further highlights the dramatic impacts Polynesians and introduced predators had on New Zealand's coastal and marine biodiversity. The prehistoric presence of at least four species of Leucocarbo shag on mainland NZ further highlights its status as a biodiversity hotspot for Phalacrocoracidae.

Population-genetic models of sex-limited genomic imprinting.

Genomic imprinting is a form of epigenetic modification involving parent-of-origin-dependent gene expression, usually the inactivation of one gene copy in some tissues, at least, for some part of the diploid life cycle. Occurring at a number of loci in mammals and flowering plants, this mode of non-Mendelian expression can be viewed more generally as parentally-specific differential gene expression. The effects of natural selection on genetic variation at imprinted loci have previously been examined in a several population-genetic models. Here we expand the existing one-locus, two-allele population-genetic models of viability selection with genomic imprinting to include sex-limited imprinting, i.e., imprinted expression occurring only in one sex, and differential viability between the sexes. We first consider models of complete inactivation of either parental allele and these models are subsequently generalized to incorporate differential expression. Stable polymorphic equilibrium was possible without heterozygote advantage as observed in some prior models of imprinting in both sexes. In contrast to these latter models, in the sex-limited case it was critical whether the paternally inherited or maternally inherited allele was inactivated. The parental origin of inactivated alleles had a different impact on how the population responded to the different selection pressures between the sexes. Under the same fitness parameters, imprinting in the other sex altered the number of possible equilibrium states and their stability. When the parental origin of imprinted alleles and the sex in which they are inactive differ, an allele cannot be inactivated in consecutive generations. The system dynamics became more complex with more equilibrium points emerging. Our results show that selection can interact with epigenetic factors to maintain genetic variation in previously unanticipated ways.

The Selective Maintenance of Allelic Variation Under Generalized Dominance.

Simple models of viability selection acting on variation at a single diploid locus only maintain multiple alleles for very restricted sets of fitnesses. Most of these models assume that fitnesses are independent, even if the genotypes share alleles. Here, we extend this result to a model with generalized dominance interactions, in which fitnesses are strongly affected by what we call the "primary effects" of the genotype's component alleles, so that genotypes with shared alleles have correlated fitnesses. Nevertheless, in keeping with previously reported results, we also show that such fitness sets are easily constructed over time if recurrent mutation is occurring simultaneously. We find that such models maintain less variation over time than do (previous) models with independently sampled fitnesses, especially when the effects of genetic drift are taken into account. We also show that there is a weak tendency for greater weighting of primary effects to evolve over time.