When Phenotypes Do Not Match Genotypes—Unexpected Phenotypic Diversity and Potential Environmental Constraints in Icelandic Stickleback

Divergent lateral plate phenotypes in stickleback represent one of only a few cases known, where a single gene underlies the phenotype under divergent selection between different habitats. However, the selection pressures leading to the repeated loss of lateral plates in freshwater are still not well understood. By genotyping 838 individuals from 9 independently colonized lakes and 1 marine population in Iceland, we found 1) that only in some lakes are phenotypes associated with the expected genotype and 2) that the independent repeated occurrence of a rarely described plate phenotype is expressed in the absence of an allele that is usually associated with this phenotype. This suggests that either other genes such as modifiers might be under divergent selection between lakes or that lateral plate expression in these populations is restricted due to environmental constraint

Predators, reproductive parasites, and the persistence of poor males on leks

Lekking males are thought to face strong directional selection on secondary sexual traits. How variation in male traits can persist under these conditions remains problematic (the lek paradox). Here, we present several game-theoretic models that show that avoidance of costly and mobile predators, sneakers, or brood parasites (enemies) leads to variation in female choice. This can result in maintenance of variation in male quality. "Enemies” will congregate around higher quality males. Females must then trade-off the benefits of mating with high-quality males against the increased risk of enemies. At equilibrium, the models predict a positive correlation between the quality of a male and the proportions of both enemies and females visiting him. In the first model, we use this framework to predict the lowest quality male on the lek that will receive any matings. In the second model, we examine the influence of this female-enemy game on the maintenance of variation in male quality. Low-quality males are likely to persist when enemies are costly to females or occur at high density, and when there is some spatial structure on the lek, so that neighboring males are typically of similar quality. If enemies are more costly to males than to females, high-quality males may benefit from receiving fewer female visits. In the third model, we consider the special case when enemies are male reproductive parasites. These models illustrate the importance of considering the simultaneous decisions of multiple players in mate choice game

Little evidence for a selective advantage of armour-reduced threespined stickleback individuals in an invertebrate predation experiment

The repeated colonization of freshwater habitats by the ancestrally marine threespined stickleback Gasterosteus aculeatus has been associated with many instances of parallel reduction in armour traits, most notably number of lateral plates. The change in predation regime from marine systems, dominated by gape-limited predators such as piscivorous fishes, to freshwater habitats where grappling invertebrate predators such as insect larvae can dominate the predation regime, has been hypothesized as a driving force. Here we experimentally test the hypothesis that stickleback with reduced armour possess a selective advantage in the face of predation by invertebrates, using a natural population of stickleback that is highly polymorphic for armour traits and a common invertebrate predator from the same location. Our results provide no compelling evidence for selection in this particular predator-prey interaction. We suggest that the postulated selective advantage of low armour in the face of invertebrate predation may not be universa

Hotshots, hot spots, and female preference: exploring lek formation models with a bower-building cichlid fish

In many animals, males congregate in leks that females visit for the sole purpose of mating. We observed male and female behavior on 3 different-sized leks of the bower-building cichlid fish Nyassachromis cf. microcephalus to test predictions of 3 prominent lek models: the "hotshot,” "hot spot,” and "female preference” models. In this system, we were able to refine these predictions by distinguishing between indirect mate choice, by which females restrict their set of potential mates in the absence of individual male assessment, and direct mate choice, by which females assess males and their territories through dyadic behavioral interactions. On no lek were males holding central territories favored by indirect or direct mate choice, contrary to the prediction of the hotshot model that leks form because inferior males establish territories surrounding hotshot males preferred by females. Average female encounter rate of males increased with lek size, a pattern typically interpreted as evidence that leks form through female preference for lekking males, rather than because males congregate in hot spots of high female density. Female propensity to engage in premating behavior once courted did not increase with lek size, suggesting female preference for males on larger leks operated through indirect choice rather than direct choice based on individual assessment. The frequency of male-male competitive interactions increased with lek size, whereas their foraging rate decreased, implying a cost to males maintaining territories on larger leks. Together these data most strongly support the female preference model, where females may benefit through indirect mate choice for males able to meet the competitive cost of occupying larger lek

Female mouthbrooders in control of pre- and postmating sexual selection

The fertilization mode determines which sex has greater control over the offspring's sires. With internal fertilization, females can strongly influence the chances of different males' ejaculates to fertilize their eggs by the postmating sexual selection process referred to as cryptic female choice. In contrast, when fertilization is external and multiple males compete in this process, the outcome of pre- and postmating sexual selection is largely determined by the competitive quality of males and their sperm. Intermediate modes of fertilization as found in mouthbrooding fishes might allow for a greater maternal influence on her offspring's sire. Here, we show that in the maternal mouthbrooder Ophthalmotilapia ventralis, females collect sperm from different males in their mouth, and males can successfully fertilize eggs even if the female did not lay eggs with them. In the field, 25 of 30 clutches had multiple sires, and the fertilization success was significantly biased toward particular males in most clutches. A mate choice experiment revealed that females prefer to spawn with males possessing strongly elongated pelvic fins, a conspicuous secondary sexual character of males in this cichlid. Additionally, the body length of males partly explained their success in sperm competition within the females' mouth, a factor without apparent influence on female choice of partners with which to lay eggs. Hence, successful sires are determined by a 2-step process that is largely under female control; females select which males to spawn with and from which males they collect additional ejaculates for the subsequent sperm competition in their mout

Genomic landscape of early ecological speciation initiated by selection on nuptial color.

Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment-dependent sexual selection has played an important role. Here, we describe a very young (~90 years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat color and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American Westcoast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat color and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defense or swimming performance. Using genome-wide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of color. Our results suggest that phenotypic and multi-chromosome genomic divergence of these morphs was driven by environment-dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry. This article is protected by copyright. All rights reserved

A Dense Linkage Map of Lake Victoria Cichlids Improved the Pundamilia Genome Assembly and Revealed a Major QTL for Sex-Determination.

Genetic linkage maps are essential for comparative genomics, high quality genome sequence assembly and fine scale quantitative trait locus (QTL) mapping. In the present study we identified and genotyped markers via restriction-site associated DNA (RAD) sequencing and constructed a genetic linkage map based on 1,597 SNP markers of an interspecific F2 cross of two closely related Lake Victoria cichlids (Pundamilia pundamilia and P sp. 'red head'). The SNP markers were distributed on 22 linkage groups and the total map size was 1,594 cM with an average marker distance of 1.01 cM. This high-resolution genetic linkage map was used to anchor the scaffolds of the Pundamilia genome and estimate recombination rates along the genome. Via QTL mapping we identified a major QTL for sex in a ∼1.9 Mb region on Pun-LG10, which is homologous to Oreochromis niloticus LG 23 (Ore-LG23) and includes a well-known vertebrate sex-determination gene (amh)

Little evidence for a selective advantage of armour-reduced threespined stickleback individuals in an invertebrate predation experiment

The repeated colonization of freshwater habitats by the ancestrally marine threespined stickleback Gasterosteus aculeatus has been associated with many instances of parallel reduction in armour traits, most notably number of lateral plates. The change in predation regime from marine systems, dominated by gape-limited predators such as piscivorous fishes, to freshwater habitats where grappling invertebrate predators such as insect larvae can dominate the predation regime, has been hypothesized as a driving force. Here we experimentally test the hypothesis that stickleback with reduced armour possess a selective advantage in the face of predation by invertebrates, using a natural population of stickleback that is highly polymorphic for armour traits and a common invertebrate predator from the same location. Our results provide no compelling evidence for selection in this particular predator–prey interaction. We suggest that the postulated selective advantage of low armour in the face of invertebrate predation may not be universal

The European Reference Genome Atlas: piloting a decentralised approach to equitable biodiversity genomics.

ABSTRACT: A global genome database of all of Earth’s species diversity could be a treasure trove of scientific discoveries. However, regardless of the major advances in genome sequencing technologies, only a tiny fraction of species have genomic information available. To contribute to a more complete planetary genomic database, scientists and institutions across the world have united under the Earth BioGenome Project (EBP), which plans to sequence and assemble high-quality reference genomes for all ∼1.5 million recognized eukaryotic species through a stepwise phased approach. As the initiative transitions into Phase II, where 150,000 species are to be sequenced in just four years, worldwide participation in the project will be fundamental to success. As the European node of the EBP, the European Reference Genome Atlas (ERGA) seeks to implement a new decentralised, accessible, equitable and inclusive model for producing high-quality reference genomes, which will inform EBP as it scales. To embark on this mission, ERGA launched a Pilot Project to establish a network across Europe to develop and test the first infrastructure of its kind for the coordinated and distributed reference genome production on 98 European eukaryotic species from sample providers across 33 European countries. Here we outline the process and challenges faced during the development of a pilot infrastructure for the production of reference genome resources, and explore the effectiveness of this approach in terms of high-quality reference genome production, considering also equity and inclusion. The outcomes and lessons learned during this pilot provide a solid foundation for ERGA while offering key learnings to other transnational and national genomic resource projects.info:eu-repo/semantics/publishedVersio

Ecological character displacement among Nothobranchius annual killifishes in Tanzania.

Divergent ecological character displacement (ECD) is the competition-driven divergence in resource use-related phenotypic traits between coexisting species. It is considered one of the primary drivers of ecological diversification and adaptive radiation. We analyzed phenotypic and ecological variation in two African annual killifish species of the genus Nothobranchius; N. eggersi and N. melanospilus in sympatry and N. melanospilus in allopatry. Our aim was to test if allopatric and sympatric populations of N. melanospilus differ morphologically from each other and from N. eggersi, and examine if these differences are consistent with the predictions of ECD. We find that sympatric N. melanospilus differ from allopatric N. melanospilus and differ from N. eggersi more strongly than the latter. Our data satisfy four criteria for demonstrating ECD: Differences in phenotypes between allopatric and sympatric N. melanospilus are greater than expected by chance; the divergence pattern between allopatric and sympatric N. melanospilus results from an evolutionary shift rather than from ecological sorting; morphological differences observed reflect differences in resource use and, lastly, sites of allopatry and sympatry do not differ in food resource availability or other ecological conditions. Our results suggest that competition is the main driver of the observed divergence between two N. melanospilus populations