Extensive variation in germline de novo mutations in Poecilia reticulata.

The rate of germline mutation is fundamental to evolutionary processes, as it generates the variation upon which selection acts. The guppy, Poecilia reticulata, is a model of rapid adaptation, however the relative contribution of standing genetic variation versus de novo mutation (DNM) to evolution in this species remains unclear. Here, we use pedigree-based approaches to quantify and characterize germline DNMs in three large guppy families. Our results suggest germline mutation rate in the guppy varies substantially across individuals and families. Most DNMs are shared across multiple siblings, suggesting they arose during early embryonic development. DNMs are randomly distributed throughout the genome, and male-biased mutation rate is low, as would be expected from the short guppy generation time. Overall, our study shows remarkable variation in germline mutation rate and provides insights into rapid evolution of guppies.

Evolutionary History of the Poecilia picta Sex Chromosomes.

The degree of divergence between the sex chromosomes is not always proportional to their age. In poeciliids, four closely related species all exhibit a male heterogametic sex chromosome system on the same linkage group, yet show a remarkable diversity in X and Y divergence. In Poecilia reticulata and P. wingei, the sex chromosomes remain homomorphic, yet P. picta and P. parae have a highly degraded Y chromosome. To test alternative theories about the origin of their sex chromosomes, we used a combination of pedigrees and RNA-seq data from P. picta families in conjunction with DNA-seq data collected from P. reticulata, P. wingei, P. parae, and P. picta. Phylogenetic clustering analysis of X and Y orthologs, identified through segregation patterns, and their orthologous sequences in closely related species demonstrates a similar time of origin for both the P. picta and P. reticulata sex chromosomes. We next used k-mer analysis to identify shared ancestral Y sequence across all four species, suggesting a single origin to the sex chromosome system in this group. Together, our results provide key insights into the origin and evolution of the poeciliid Y chromosome and illustrate that the rate of sex chromosome divergence is often highly heterogenous, even over relatively short evolutionary time frames.

Extreme Y chromosome polymorphism corresponds to five male reproductive morphs of a freshwater fish.

Loss of recombination between sex chromosomes often depletes Y chromosomes of functional content and genetic variation, which might limit their potential to generate adaptive diversity. Males of the freshwater fish Poecilia parae occur as one of five discrete morphs, all of which shoal together in natural populations where morph frequency has been stable for over 50 years. Each morph uses a different complex reproductive strategy and morphs differ dramatically in colour, body size and mating behaviour. Morph phenotype is passed perfectly from father to son, indicating there are five Y haplotypes segregating in the species, which encode the complex male morph characteristics. Here, we examine Y diversity in natural populations of P. parae. Using linked-read sequencing on multiple P. parae females and males of all five morphs, we find that the genetic architecture of the male morphs evolved on the Y chromosome after recombination suppression had occurred with the X. Comparing Y chromosomes between each of the morphs, we show that, although the Ys of the three minor morphs that differ in colour are highly similar, there are substantial amounts of unique genetic material and divergence between the Ys of the three major morphs that differ in reproductive strategy, body size and mating behaviour. Altogether, our results suggest that the Y chromosome is able to overcome the constraints of recombination loss to generate extreme diversity, resulting in five discrete Y chromosomes that control complex reproductive strategies.

Divergence and Remarkable Diversity of the Y Chromosome in Guppies.

The guppy sex chromosomes show an extraordinary diversity in divergence across populations and closely related species. In order to understand the dynamics of the guppy Y chromosome, we used linked-read sequencing to assess Y chromosome evolution and diversity across upstream and downstream population pairs that vary in predator and food abundance in three replicate watersheds. Based on our population-specific genome assemblies, we first confirmed and extended earlier reports of two strata on the guppy sex chromosomes. Stratum I shows significant accumulation of male-specific sequence, consistent with Y divergence, and predates the colonization of Trinidad. In contrast, Stratum II shows divergence from the X, but no Y-specific sequence, and this divergence is greater in three replicate upstream populations compared with their downstream pair. Despite longstanding assumptions that sex chromosome recombination suppression is achieved through inversions, we find no evidence of inversions associated with either Stratum I or Stratum II. Instead, we observe a remarkable diversity in Y chromosome haplotypes within each population, even in the ancestral Stratum I. This diversity is likely due to gradual mechanisms of recombination suppression, which, unlike an inversion, allow for the maintenance of multiple haplotypes. In addition, we show that this Y diversity is dominated by low-frequency haplotypes segregating in the population, suggesting a link between haplotype diversity and female preference for rare Y-linked color variation. Our results reveal the complex interplay between recombination suppression and Y chromosome divergence at the earliest stages of sex chromosome divergence.

High-resolution characterization of male ornamentation and re-evaluation of sex linkage in guppies.

Coloration plays a key role in the ecology of many species, influencing how an organism interacts with its environment, other species and conspecifics. Guppies are sexually dimorphic, with males displaying sexually selected coloration resulting from female preference. Previous work has suggested that much of guppy colour pattern variation is Y-linked. However, it remains unclear how many individual colour patterns are Y-linked in natural populations as much of the previous work has focused on phenotypes either not found in the wild, or aggregate measures such as total colour area. Moreover, ornaments have traditionally been identified and delineated by hand, and computational methods now make it possible to extract pixels and identify ornaments with automated methods, reducing the potential for human bias. Here we developed a pipeline for semi-automated ornament identification and high-resolution image analysis of male guppy colour patterns and applied it to a multigenerational pedigree. Our results show that loci controlling the presence or the absence of individual male ornaments in our population are not predominantly Y-linked. However, we find that ornaments of similar colour are not independent of each other, and modifier loci that affect whole animal coloration appear to be at least partially Y-linked. Considering these results, Y-linkage of individual ornaments may not be important in driving colour changes in natural populations of guppies, or in expansions of the non-recombining Y region, while Y-linked modifier loci that affect aggregate traits may well play an important role.

Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry.

Convergent evolution can occur through different genetic mechanisms in different species. It is now clear that convergence at the genetic level is also widespread, and can be caused by either (i) parallel genetic evolution, where independently evolved convergent mutations arise in different populations or species, or (ii) collateral evolution in which shared ancestry results from either ancestral polymorphism or introgression among taxa. The adaptive radiation of Heliconius butterflies shows color pattern variation within species, as well as mimetic convergence between species. Using comparisons from across multiple hybrid zones, we use signals of shared ancestry to identify and refine multiple putative regulatory elements in Heliconius melpomene and its comimics, Heliconius elevatus and Heliconius besckei, around three known major color patterning genes: optix, WntA, and cortex While we find that convergence between H. melpomene and H. elevatus is caused by a complex history of collateral evolution via introgression in the Amazon, convergence between these species in the Guianas appears to have evolved independently. Thus, we find adaptive convergent genetic evolution to be a key driver of regulatory changes that lead to rapid phenotypic changes. Furthermore, we uncover evidence of parallel genetic evolution at some loci around optix and WntA in H. melpomene and its distant comimic Heliconius erato Ultimately, we show that all three of convergence, conservation, and novelty underlie the modular architecture of Heliconius color pattern mimicry.

Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers.

Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

Geographic contrasts between pre- and postzygotic barriers are consistent with reinforcement in Heliconius butterflies.

Identifying the traits causing reproductive isolation and the order in which they evolve is fundamental to understanding speciation. Here, we quantify prezygotic and intrinsic postzygotic isolation among allopatric, parapatric, and sympatric populations of the butterflies Heliconius elevatus and Heliconius pardalinus. Sympatric populations from the Amazon (H. elevatus and H. p. butleri) exhibit strong prezygotic isolation and rarely mate in captivity; however, hybrids are fertile. Allopatric populations from the Amazon (H. p. butleri) and Andes (H. p. sergestus) mate freely when brought together in captivity, but the female F1 hybrids are sterile. Parapatric populations (H. elevatus and H. p. sergestus) exhibit both assortative mating and sterility of female F1s. Assortative mating in sympatric populations is consistent with reinforcement in the face of gene flow, where the driving force, selection against hybrids, is due to disruption of mimicry and other ecological traits rather than hybrid sterility. In contrast, the lack of assortative mating and hybrid sterility observed in allopatric populations suggests that geographic isolation enables the evolution of intrinsic postzygotic reproductive isolation. Our results show how the types of reproductive barriers that evolve between species may depend on geography.

The genetic architecture of adaptation: convergence and pleiotropy in Heliconius wing pattern evolution.

Unravelling the genetic basis of adaptive traits is a major challenge in evolutionary biology. Doing so informs our understanding of evolution towards an adaptive optimum, the distribution of locus effect sizes, and the influence of genetic architecture on the evolvability of a trait. In the Müllerian co-mimics Heliconius melpomene and Heliconius erato some Mendelian loci affecting mimicry shifts are well known. However, several phenotypes in H. melpomene remain to be mapped, and the quantitative genetics of colour pattern variation has rarely been analysed. Here we use quantitative trait loci (QTL) analyses of crosses between H. melpomene races from Peru and Suriname to map, for the first time, the control of the broken band phenotype to WntA and identify a ~100 kb region controlling this variation. Additionally, we map variation in basal forewing red-orange pigmentation to a locus centred around the gene ventral veins lacking (vvl). The locus also appears to affect medial band shape variation as it was previously known to do in H. erato. This adds to the list of homologous regions controlling convergent phenotypes between these two species. Finally we show that Heliconius wing-patterning genes are strikingly pleiotropic among wing pattern traits. Our results demonstrate how genetic architecture can shape, aid and constrain adaptive evolution.

Shared and Species-Specific Patterns of Nascent Y Chromosome Evolution in Two Guppy Species.

Sex chromosomes form once recombination is halted around the sex-determining locus between a homologous pair of chromosomes, resulting in a male-limited Y chromosome. We recently characterized the nascent sex chromosome system in the Trinidadian guppy (Poeciliareticulata). The guppy Y is one of the youngest animal sex chromosomes yet identified, and therefore offers a unique window into the early evolutionary forces shaping sex chromosome formation, particularly the rate of accumulation of repetitive elements and Y-specific sequence. We used comparisons between male and female genomes in P. reticulata and its sister species, Endler’s guppy (P. wingei), which share an ancestral sex chromosome, to identify male-specific sequences and to characterize the degree of differentiation between the X and Y chromosomes. We identified male-specific sequence shared between P. reticulata and P. wingei consistent with a small ancestral non-recombining region. Our assembly of this Y-specific sequence shows substantial homology to the X chromosome, and appears to be significantly enriched for genes implicated in pigmentation. We also found two plausible candidates that may be involved in sex determination. Furthermore, we found that the P. wingei Y chromosome exhibits a greater signature of repetitive element accumulation than the P. reticulata Y chromosome. This suggests that Y chromosome divergence does not necessarily correlate with the time since recombination suppression. Overall, our results reveal the early stages of Y chromosome divergence in the guppy.

Engaging with peri-urban woodlands in England: the contribution to people's health and well-being and implications for future management.

In this paper we engage with debates concerning people and their contact with the natural environment as part of everyday life drawing on Irwin's ideas of co-construction and Gibson's theory of affordances. We focus on peri-urban woodlands in England as important places where people can interact with nature for health and well-being. Qualitative data were collected in situ via walks in the woods, focus group discussions and photo elicitation, with a sample of 49 people. These methods provide rich data on the wide range of meanings associated with woodlands that can have a perceived impact on people's health and well-being. The findings link to contemporary debates about health, well-being and ecosystem services. We explore the inter-play between attributes of the physical environment and the range of facilities provided to enable access, social interactions and the benefits people attribute to their woodland experiences. We conclude that peri-urban woodlands can clearly contribute to self-reported health and well-being in multiple ways, and that organized activities can be important for those who face barriers to accessing woodlands. A strong message emerging from the research is the opportunity afforded by woodlands for social connections with others, as well as the provision of a range of sensory benefits and opportunities to observe and enjoy seasonal change in woodlands. Mental restoration via connection with nature also emerged as important, confirming previous research.

Regional impact assessment of land use scenarios in developing countries using the FoPIA approach: findings from five case studies.

The impact of land use changes on sustainable development is of increasing interest in many regions of the world. This study aimed to test the transferability of the Framework for Participatory Impact Assessment (FoPIA), which was originally developed in the European context, to developing countries, in which lack of data often prevents the use of data-driven impact assessment methods. The core aspect of FoPIA is the stakeholder-based assessment of alternative land use scenarios. Scenario impacts on regional sustainability are assessed by using a set of nine regional land use functions (LUFs), which equally cover the economic, social and environmental dimensions of sustainability. The cases analysed in this study include (1) the alternative spatial planning policies around the Merapi volcano and surrounding areas of Yogyakarta City, Indonesia; (2) the large-scale afforestation of agricultural areas to reduce soil erosion in Guyuan, China; (3) the expansion of soil and water conservation measures in the Oum Zessar watershed, Tunisia; (4) the agricultural intensification and the potential for organic agriculture in Bijapur, India; and (5) the land degradation and land conflicts resulting from land division and privatisation in Narok, Kenya. All five regions are characterised by population growth, partially combined with considerable economic development, environmental degradation problems and social conflicts. Implications of the regional scenario impacts as well as methodological aspects are discussed. Overall, FoPIA proved to be a useful tool for diagnosing regional human-environment interactions and for supporting the communication and social learning process among different stakeholder groups.

Participatory impact assessment of soil and water conservation scenarios in Oum Zessar watershed, Tunisia.

Environmental threats and progressive degradation of natural resources are considered critical impediments to sustainable development. This paper reports on a participatory impact assessment of alternative soil and water conservation (SWC) scenarios in the Oum Zessar watershed, Tunisia. The first objective was to assess the impact of three SWC scenarios on key social, economic and environmental land use functions. The second objective was to test and evaluate the applicability of the 'Framework for Participatory Impact Assessment (FoPIA)' for assessing scenario impacts in the context of a developing country, in this case Tunisia. The assessed scenarios included: the originally planned SWC policy implementation at 85 % coverage of arable land of the watershed, the current implementation (70 %), and a hypothetical expansion of SWC measures to the entire watershed (100 %). Our results suggest that implementation of the SWC policy at 100 % coverage of arable land achieves the maximum socioeconomic benefit. However, if stakeholders' preferences regarding land use functions are taken into account, and considering the fact that the implementation of SWC measures also implies some negative changes to traditional landscapes and the natural system, SWC implementation at 85 % coverage of arable land might be preferable. The FoPIA approved to be a useful tool for conducting a holistic sustainability impact assessment of SWC scenarios and for studying the most intriguing sustainability problems while providing possible recommendations towards sustainable development. We conclude that participatory impact assessment contributes to an enhanced regional understanding of key linkages between policy effects and sustainable development, which provides the foundation for improved policy decision making.