Ecological, evolutionary and human-mediated determinants of poeciliid species richness on Caribbean islands

Aim: The theory of island biogeography provides a predictive framework relating species richness to island size and distance from the mainland. However, the theory as originally formulated does not necessarily scale to large islands and continental landmasses that are capable of generating species through in situ speciation (rather than entirely by colonization), nor does it necessarily account for how human introduction of species alters traditional biogeographical patterns. Here, we examine the ecological (colonization and extinction), evolutionary (in situ speciation) and human-mediated (deliberate introductions) determinants of species richness in a taxonomic group that has undergone a radiation on Caribbean islands: live-bearing fishes of the family Poeciliidae. Location: The Caribbean. Methods: We created a database of both native and introduced poeciliid species occurrence on Caribbean islands through literature review, and estimated the number of colonizations versus speciation events on each island using a molecular phylogeny. Linear regression and other statistical tests were used to explore species–area and species–isolation relationships. Results: Species richness on small islands results entirely from colonization and does not significantly increase with island area, whereas on larger islands species richness increases dramatically as a function of area due primarily to in situ speciation. Poeciliid fishes have been introduced widely, both as a by-product of their popularity in the aquarium hobby and as a means of mosquito control. We show that such establishments have occurred disproportionately on islands depauperate in native species, and that introduced species richness is positively correlated with economic interconnectedness (shipping traffic) and human population size. Main conclusions: On large Caribbean islands in situ speciation has elevated the number of poeciliid species beyond that predicted from ecological processes alone. Introduced species significantly alter biogeographical patterns

Sex-Specific Differences in Shoaling Affect Parasite Transmission in Guppies

Background: Individuals have to trade-off the costs and benefits of group membership during shoaling behaviour. Shoaling can increase the risk of parasite transmission, but this cost has rarely been quantified experimentally. Guppies (Poecilia reticulata) are a model system for behavioural studies, and they are commonly infected by gyrodactylid parasites, notorious fish pathogens that are directly transmitted between guppy hosts. Methodology/Principal Findings:Parasite transmission in single sex shoals of male and female guppies were observed using an experimental infection of Gyrodactylus turnbulli. Parasite transmission was affected by sex-specific differences in host behaviour, and significantly more parasites were transmitted when fish had more frequent and more prolonged contact with each other. Females shoaled significantly more than males and had a four times higher risk to contract an infection. Conclusions/Significance: Intersexual differences in host behaviours such as shoaling are driven by differences in natural and sexual selection experienced by both sexes. Here we show that the potential benefits of an increased shoaling tendency are traded off against increased risks of contracting an infectious parasite in a group-living species

Manipulation of feeding regime alters sexual dimorphism for lifespan and reduces sexual conflict in Drosophila melanogaster

Sexual dimorphism for lifespan (SDL) is widespread, but poorly understood. A leading hypothesis, which we test here, is that strong SDL can reduce sexual conflict, by allowing each sex to maximise its sex-specific fitness. We used replicated experimental evolution lines of the fruit fly, Drosophila melanogaster, which had been maintained for over 360 generations on either unpredictable ‘Random’ or predictable ‘Regular’ feeding regimes. This evolutionary manipulation of feeding regime led to robust, enhanced SDL in Random over control, Regular lines. Enhanced SDL was associated with a significant increase in the fitness of focal males, tested with wild type females. This was due to sex-specific changes to male life history, manifested as increased early reproductive output and reduced survival. In contrast, focal female fitness, tested with wild type males, did not differ across regimes. Hence increased SDL was associated with a reduction in sexual conflict, which increased male fitness and maintained fitness in females. Differences in SDL were not associated with developmental time or developmental survival. Overall, the results showed that the expression of enhanced SDL, resulting from experimental evolution of feeding regimes, was associated with male-specific changes in life history, leading to increased fitness and reduced sexual conflict

A climate for contemporary evolution

A new study of divergence in freshwater fish provides strong evidence of rapid, temperature-mediated adaptation. This study is particularly important in the ongoing debate over the extent and significance of evolutionary response to climate change because divergence has occurred in relatively few generations in spite of ongoing gene flow and in the aftermath of a significant genetic bottleneck, factors that have previously been considered obstacles to evolution. Climate change may thus be more likely to foster contemporary evolutionary responses than has been anticipated, and I argue here for the importance of investigating their possible occurrence

Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)

This is the final version. Available on open access from Wiley via the DOI in this recordData archiving: The data that support these findings are openly available at: European Nucleotide Archive (https://www.ebi.ac.uk/ena/ browser/home)—reference numbers: PRJEB42705 (all introduction populations) and PRJEB10680 (GHP). All scripts and associated data are available on Github repository: mapping and SNP calling (https://github.com/josieparis/gatk-snp-calling); population genomics and haplotype scans (https://github.com/ bfraser-commits/Rapid_genomic_adaptation_guppies); the software for multivariate AF analyses (AF-vapeR) (https://github. com/JimWhiting91/afvaper); and simulation analyses (https:// github.com/JimWhiting91/fibr_simulations).Although rapid phenotypic evolution has been documented often, the genomic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high-predation (HP) to low-predation (LP) environments have been shown to evolve toward the phenotypes of naturally colonized LP populations in as few as eight generations. These changes persist in common garden experiments, indicating that they have a genetic basis. Here, we report results of whole genome variation in four experimental populations colonizing LP sites along with the corresponding HP source population. We examined genome-wide patterns of genetic variation to estimate past demography and used a combination of genome scans, forward simulations, and a novel analysis of allele frequency change vectors to uncover the signature of selection. We detected clear signals of population growth and bottlenecks at the genome-wide level that matched the known history of population numbers. We found a region on chromosome 15 under strong selection in three of the four populations and with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome-wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments.Max Planck SocietyEuropean Research Council (ERC)Natural Environment Research Council (NERC)University of SussexUniversity of ExeterNational Science Foundation (NSF

Sex-specific local life-history adaptation in surface- and cave-dwelling Atlantic mollies (Poecilia mexicana)

Cavefishes have long been used as model organisms showcasing adaptive diversification, but does adaptation to caves also facilitate the evolution of reproductive isolation from surface ancestors? We raised offspring of wild-caught surface- and cave-dwelling ecotypes of the neotropical fish Poecilia mexicana to sexual maturity in a 12-month common garden experiment. Fish were raised under one of two food regimes (high vs. low), and this was crossed with differences in lighting conditions (permanent darkness vs. 12:12 h light:dark cycle) in a 2 × 2 factorial design, allowing us to elucidate potential patterns of local adaptation in life histories. Our results reveal a pattern of sex-specific local life-history adaptation: Surface molly females had the highest fitness in the treatment best resembling their habitat of origin (high food and a light:dark cycle), and suffered from almost complete reproductive failure in darkness, while cave molly females were not similarly affected in any treatment. Males of both ecotypes, on the other hand, showed only weak evidence for local adaptation. Nonetheless, local life-history adaptation in females likely contributes to ecological diversification in this system and other cave animals, further supporting the role of local adaptation due to strong divergent selection as a major force in ecological speciation

Night Shift: Expansion of Temporal Niche Use Following Reductions in Predator Density

Predation shapes many fundamental aspects of ecology. Uncertainty remains, however, about whether predators can influence patterns of temporal niche construction at ecologically relevant timescales. Partitioning of time is an important mechanism by which prey avoid interactions with predators. However, the traits that control a prey organism's capacity to operate during a particular portion of the diel cycle are diverse and complex. Thus, diel prey niches are often assumed to be relatively unlikely to respond to changes in predation risk at short timescales. Here we present evidence to the contrary. We report results that suggest that the anthropogenic depletion of daytime active predators (species that are either diurnal or cathemeral) in a coral reef ecosystem is associated with rapid temporal niche expansions in a multi-species assemblage of nocturnal prey fishes. Diurnal comparisons of nocturnal prey fish abundance in predator rich and predator depleted reefs at two atolls revealed that nocturnal fish were approximately six (biomass) and eight (density) times more common during the day on predator depleted reefs. Amongst these, the prey species that likely were the most specialized for nocturnal living, and thus the most vulnerable to predation (i.e. those with greatest eye size to body length ratio), showed the strongest diurnal increases at sites where daytime active predators were rare. While we were unable to determine whether these observed increases in diurnal abundance by nocturnal prey were the result of a numerical or behavioral response, either effect could be ecologically significant. These results raise the possibility that predation may play an important role in regulating the partitioning of time by prey and that anthropogenic depletions of predators may be capable of causing rapid changes to key properties of temporal community architecture

The genome of the Trinidadian guppy, Poecilia reticulata, and variation in the Guanapo population

For over a century, the live bearing guppy, Poecilia reticulata, has been used to study sexual selection as well as local adaptation. Natural guppy populations differ in many traits that are of intuitively adaptive significance such as ornamentation, age at maturity, brood size and body shape. Water depth, light supply, food resources and predation regime shape these traits, and barrier waterfalls often separate contrasting environments in the same river. We have assembled and annotated the genome of an inbred single female from a high-preda- tion site in the Guanapo drainage. The final assembly comprises 731.6 Mb with a scaffold N50 of 5.3 MB. Scaffolds were mapped to linkage groups, placing 95% of the genome assembly on the 22 autosomes and the X-chromosome. To investigate genetic variation in the population used for the genome assembly, we sequenced 10 wild caught male individu- als. The identified 5 million SNPs correspond to an average nucleotide diversity (π) of 0.0025. The genome assembly and SNP map provide a rich resource for investigating adap- tation to different predation regimes. In addition, comparisons with the genomes of other Poeciliid species, which differ greatly in mechanisms of sex determination and maternal resource allocation, as well as comparisons to other teleost genera can begin to reveal how live bearing evolved in teleost fish

Predation by Bears Drives Senescence in Natural Populations of Salmon

Classic evolutionary theory predicts that populations experiencing higher rates of environmentally caused (“extrinsic”) mortality should senesce more rapidly, but this theory usually neglects plausible relationships between an individual's senescent condition and its susceptibility to extrinsic mortality. We tested for the evolutionary importance of this condition dependence by comparing senescence rates among natural populations of sockeye salmon (Oncorhynchus nerka) subject to varying degrees of predation by brown bears (Ursus arctos). We related senescence rates in six populations to (1) the overall rate of extrinsic mortality, and (2) the degree of condition dependence in this mortality. Senescence rates were determined by modeling the mortality of individually-tagged breeding salmon at each site. The overall rate of extrinsic mortality was estimated as the long-term average of the annual percentage of salmon killed by bears. The degree of condition dependence was estimated as the extent to which bears killed salmon that exhibited varying degrees of senescence. We found that the degree of condition dependence in extrinsic mortality was very important in driving senescence: populations where bears selectively killed fish showing advanced senescence were those that senesced least rapidly. The overall rate of extrinsic mortality also contributed to among-population variation in senescence-but to a lesser extent. Condition-dependent susceptibility to extrinsic mortality should be incorporated more often into theoretical models and should be explicitly tested in natural populations