Reevaluating claims of ecological speciation in Halichoeres bivittatus

Understanding the role of ecological processes in speciation has become one of the most active areas of research in marine population biology in recent decades. The traditional view was that allopatry was the primary driver of speciation in marine taxa, but the geography of the marine environment and the dispersal capabilities of many marine organisms render this view somewhat questionable. One of the earliest and most highly cited empirical examples of ecological speciation with gene flow in marine fishes is that of the slippery dick wrasse, Halichoeres bivittatus. Evidence for this cryptic or incipient speciation event was primarily in the form of a deep north-south divergence in a single mitochondrial locus, combined with a finding that these two haplotypes were associated with different habitat types in the Florida Keys and Bermuda, where they overlap. Here we examine habitat assortment in the Florida Keys using a broader sampling of populations and habitat types than were available for the original study, and find no evidence to support the claim that haplotype frequencies differ between habitat types, and little evidence to support any differences between populations. These results severely undermine claims of ecological speciation with gene flow in Halichoeres bivittatus. We argue that future claims of this type should be supported by multiple lines of evidence that illuminate potential mechanisms and allow researchers to rule out alternative explanations for spatial patterns of genetic differences.

Reevaluating claims of ecological speciation in Halichoeres bivittatus

Understanding the role of ecological processes in speciation has become one of the most active areas of research in marine population biology in recent decades. The traditional view was that allopatry was the primary driver of speciation in marine taxa, but the geography of the marine environment and the dispersal capabilities of many marine organisms render this view somewhat questionable. One of the earliest and most highly cited empirical examples of ecological speciation with gene flow in marine fishes is that of the slippery dick wrasse, Halichoeres bivittatus. Evidence for this cryptic or incipient speciation event was primarily in the form of a deep north-south divergence in a single mitochondrial locus, combined with a finding that these two haplotypes were associated with different habitat types in the Florida Keys and Bermuda, where they overlap. Here we examine habitat assortment in the Florida Keys using a broader sampling of populations and habitat types than were available for the original study, and find no evidence to support the claim that haplotype frequencies differ between habitat types, and little evidence to support any differences between populations. These results severely undermine claims of ecological speciation with gene flow in Halichoeres bivittatus. We argue that future claims of this type should be supported by multiple lines of evidence that illuminate potential mechanisms and allow researchers to rule out alternative explanations for spatial patterns of genetic differences.

Evolution of thermal physiology alters predicted species distributions under climate change

Species distribution models (SDMs) are widely adopted to predict range shifts but can be unreliable under climate change scenarios1 because they do not account for evolution. The thermal physiology of a species is a key determinant of range2,3 but the impact of thermal trait evolution on SDMs has not been addressed. We identified a genetic basis for physiological traits that evolve in response to temperature change in threespine stickleback. Using these data, we created geographic range projections under two climate change scenarios where trait data was either static (‘no evolution’ model), allowed to evolve in agreement with published evolutionary rates for the trait (‘evolution’ model)4, or allowed to evolve with the rate of evolution scaled in association with the variance that is explained by QTL (‘PVE’ model). Here, we show that incorporating these traits and their evolution into SDMs substantially altered the predicted ranges for a widespread panmictic marine population, with increases in area of over 7-fold. Evolution-informed SDMs should therefore improve the precision of forecasting range dynamics under climate change, thereby aiding in their application to management and the protection of biodiversity5-7.

Diversity and sexual dimorphism in the head lateral line system in North Sea populations of threespine sticklebacks, Gasterosteus aculeatus (Teleostei: Gasterosteidae)

The mechanosensory lateral line of fishes is a flow sensing system and supports a number of behaviors, e.g. prey detection, schooling or position holding in water currents. Differences in the neuromast pattern of this sensory system reflect adaptation to divergent ecological constraints. The threespine stickleback, Gasterosteus aculeatus, is known for its ecological plasticity resulting in three major ecotypes, a marine type, a migrating anadromous type and a resident freshwater type. We provide the first comparative study of the pattern of the head lateral line system of North Sea populations representing these three ecotypes including a brackish spawning population. We found no distinct difference in the pattern of the head lateral line system between the three ecotypes but significant differences in neuromast numbers. The anadromous and the brackish populations had distinctly less neuromasts than their freshwater and marine conspecifics. This difference in neuromast number between marine and anadromous threespine stickleback points to differences in swimming behavior. We also found sexual dimorphism in neuromast number with males having more neuromasts than females in the anadromous, brackish and the freshwater populations. But no such dimorphism occurred in the marine population. Our results suggest that the head lateral line of the three ecotypes is under divergent hydrodynamic constraints. Additionally, sexual dimorphism points to divergent niche partitioning of males and females in the anadromous and freshwater but not in the marine populations. Our findings imply careful sampling as an important prerequisite to discern especially between anadromous and marine threespine sticklebacks.

Complementarity and discriminatory power of genotype and otolith shape in describing the fine-scale population structure of an exploited fish, the common sole of the Eastern English Channel

Marine organisms show population structure at a relatively fine spatial scale, even in open habitats. The tools commonly used to assess subtle patterns of connectivity have diverse levels of resolution and can complement each other to inform on population structure. We assessed and compared the discriminatory power of genetic markers and otolith shape to reveal the population structure on evolutionary and ecological time scales of the common sole (Solea solea), living in the Eastern English Channel (EEC) stock off France and the UK. First, we genotyped fish with Single Nucleotide Polymorphisms to assess population structure at an evolutionary scale. Then, we tested for spatial segregation of the subunits using otolith shape as an integrative tracer of life history. Finally, a supervised machine learning framework was applied to genotypes and otolith phenotypes to probabilistically assign adults to subunits and assess the discriminatory power of each approach. Low but significant genetic differentiation was found among subunits. Moreover, otolith shape appeared to vary spatially, suggesting spatial population structure at fine spatial scale. However, results of the supervised discriminant analyses failed to discriminate among subunits, especially for otolith shape. We suggest that the degree of population segregation may not be strong enough to allow for robust fish assignments. Finally, this study revealed a weak yet existing metapopulation structure of common sole at the fine spatial scale of the EEC based on genotypes and otolith shape, with one subunit being more isolated. Our study argues for the use of complementary tracers to investigate marine population structure.

Evidence and population consequences of shared larval dispersal histories in a marine fish

© 2016 by the Ecological Society of America. Larval dispersal is disproportionately important for marine population ecolgy and evolution, yet our inability to track individuals severely constrains our understanding of this key process. We analyze otoliths of a small reef fish, the common triplefin ( Forsterygion lapillum ), to reconstruct individual dispersal histories and address the following questions: (1) How many discrete sets of dispersal histories (dispersal cohorts) contribute to replenishment of focal populations; (2) When do dispersal cohorts converge (a metric of shared dispersal histories among cohorts); and (3) Do these patterns predict spatiotemporal variation in larval supply? We used light traps to quantify larval supply, and otolith microstructure and microchemistry (using laser ablation inductively coupled plasma mass spectrometry; LA - ICP - MS ) to reconstruct daily environmental histories of individuals in their 30- d lead- up to settlement. Our results indicate that a variable number of dispersal cohorts replenish focal populations (range of 2-8, mean of 4.3, standard deviation of 2.8). Convergence times varied (from 0 to >30 d prior to settlement), and larval supply was negatively correlated with cohort evenness but not with the number of cohorts, or when they converged, indicating disproportionately large contributions from some cohorts (i.e., sweepstakes events). Collectively, our results suggest that larval reef fishes may variably disperse in shoals, to drive local replenishment and connectivity within a metapopulation.

Evidence and population consequences of shared larval dispersal histories in a marine fish

© 2016 by the Ecological Society of America. Larval dispersal is disproportionately important for marine population ecolgy and evolution, yet our inability to track individuals severely constrains our understanding of this key process. We analyze otoliths of a small reef fish, the common triplefin ( Forsterygion lapillum ), to reconstruct individual dispersal histories and address the following questions: (1) How many discrete sets of dispersal histories (dispersal cohorts) contribute to replenishment of focal populations; (2) When do dispersal cohorts converge (a metric of shared dispersal histories among cohorts); and (3) Do these patterns predict spatiotemporal variation in larval supply? We used light traps to quantify larval supply, and otolith microstructure and microchemistry (using laser ablation inductively coupled plasma mass spectrometry; LA - ICP - MS ) to reconstruct daily environmental histories of individuals in their 30- d lead- up to settlement. Our results indicate that a variable number of dispersal cohorts replenish focal populations (range of 2-8, mean of 4.3, standard deviation of 2.8). Convergence times varied (from 0 to >30 d prior to settlement), and larval supply was negatively correlated with cohort evenness but not with the number of cohorts, or when they converged, indicating disproportionately large contributions from some cohorts (i.e., sweepstakes events). Collectively, our results suggest that larval reef fishes may variably disperse in shoals, to drive local replenishment and connectivity within a metapopulation.

Land-Mark based morphometric and meristic variations in two congeneric hilsha population, Tenualosa ilisha and Tenualosa toli from Bangladesh water bodies

The morphometric characters are effectively used for the better differentiation among the fish population and sustainable management. The appraisal of the natural population stock and morphological variation within and between two hilsha species (Tenualosa ilisha and Tenualosa toli) from three different habitat (Coastal, riverine and marine) of Bangladesh, were investigated by applying the land mark based morphometric and meristic variation measurement methods. All data were adjusted and Univariate ANOVA, where discriminant function analysis (DFA) and principal component analysis (PCA) exhibited the divergences in eight morphometric measurements and eight truss network measurements among the three stocks of T. ilisha. The 1st DFA accounted for 89.8% & 87.4% and the second DFA resolved 10.2% and 12.6%, respectively in morphometric characteristics variation among the group studied. Scattered plotting from PCA and dendogram from cluster analysis (CA) revealed that, the river habitants were morphologically different from the coastal and marine population. Twelve of fifteen morphometric measurements and thirteen of fourteen truss network measurements showed significant differences between T. ilisha and T. toil with significant variation in meristic characters. PCA revealed 89.23% and 88.29% in case of morphometric and truss measurement respectively confirmed high degree of variations in morphological characteristics between two species. Overall, our results based on morphometrics with truss measurements together provide useful information about the morphological differentiation which will be helpful for sustainable exploration and effective management for these two species. Asian J. Med. Biol. Res. June 2020, 6(2): 265-282

Rapid Evolution of Parasite Resistance via Improved Recognition and Accelerated Immune Activation and Deactivation

ABSTRACTClosely related populations often differ in resistance to a given parasite, as measured by infection success or failure. Yet, the immunological mechanisms of these evolved differences are rarely specified. Does resistance evolve via changes to the host’s ability to recognize that an infection exists, actuate an effective immune response, or attenuate that response? We tested whether each of these phases of the host response contributed to threespine sticklebacks’ recently evolved resistance to their tapeworm Schistocephalus solidus. While marine stickleback and some susceptible lake fish permit fast-growing tapeworms, other lake populations are resistant and suppress tapeworm growth via a fibrosis response. We subjected lab-raised fish from three populations (susceptible marine ‘ancestors’, a susceptible lake, a resistant lake), to a novel immune challenge (injection of: 1) a saline control, 2) alum, a generalized pro-inflammatory adjuvant that causes fibrosis, 3) a tapeworm protein extract, and 4) a combination of alum and tapeworm protein). All three populations were capable of a robust fibrosis response to the alum treatments (but not the saline control). Yet, only the resistant population exhibited a fibrosis response to the tapeworm protein alone. Thus, these populations differed in their ability to recognize the tapeworm but shared an intact fibrosis pathway. However, the resistant population also initiated fibrosis faster, and was able to attenuate fibrosis, unlike the susceptible populations slow but longer-lasting response to alum. As fibrosis has presumed pathological side-effects, this difference may reflect adaptions to mitigate costs of immunity in the resistant population. Broadly, our results confirm that parasite detection, activation speed, and immune attenuation simultaneously contribute to adaptations to parasite infection in natural populations.IMPACT SUMMARYDramatic variation in parasite resistance is common in nature, even to the same parasite, yet we are still working to understand the mechanisms of how such differences evolve. Many evolution studies focus on the broad outcomes of infection (infected or not) when studying this question, without specifying what part of the immune response has evolved. Here, we experimentally partition different sequential stages in the host immune response (recognition, actuation, attenuation), to evaluate which stage(s) underly the evolution of host resistance to infection. This study compares three populations of threespine stickleback that naturally differ in their exposure and their ability to resist infections of a freshwater tapeworm. These include a “resistant” lake population, a “susceptible” lake population, and an ancestral marine population that is rarely exposed to the tapeworm in nature, but is susceptible when exposed in the lab. The resistant population exhibits a fibrosis immune response to infection, which has previously been linked to suppressed tapeworm growth and viability. We injected different immune challenges directly into the site of infection (peritoneal cavity) and measured the subsequent fibrosis response through time. We found that all populations were capable of producing fibrosis in response to a general immune stimulant (alum). But, only the resistant population was able to recognize and respond to tapeworm protein alone. This population also responded faster than the others, within 24 hours, and attenuated its fibrosis by 90 days post-injections whereas the other populations exhibited a slower response that did not attenuate in the study time-frame. We concluded that variation in parasite recognition, an early phase in the host response, shapes the evolution of the initiation and resolution of the physical response to infection. Broadly, our results support that parasite detection mechanisms could play a key role in the rapid evolution of parasite resistance.

Contrasting effects of coastal upwelling on growth and recruitment of nearshore Pacific rockfishes (genus Sebastes)

Knowledge of processes underlying recruitment is critical for understanding marine population dynamics and their response to ocean climate. We investigated the relationship between coastal upwelling and early life history of black rockfish (Sebastes melanops), a midwater aggregating species, and CQB rockfishes (a solitary benthic species complex including Sebastes caurinus, Sebastes maliger, and Sebastes auriculatus), between two oceanographically distinct years on the west coast of Vancouver Island, Canada. We analysed otolith microstructure to determine parturition and settlement dates, pelagic durations, and pre- and postsettlement growth rates. High CQB rockfish recruitment in 2005 was associated with prolonged downwelling and warm ocean temperatures, late parturition dates, fast presettlement growth, short pelagic durations, and small size-at-settlement. In contrast, high black rockfish recruitment in 2006 was associated with strong upwelling and cool ocean temperatures, slow presettlement growth, and protracted pelagic durations. Presettlement growth of both rockfish complexes increased with high sea surface temperature, but was unrelated to chlorophyll a concentration. Our results indicate that the same oceanographic conditions give rise to fast presettlement growth and short pelagic durations for both groups, but that different factors lead to strong recruitment in each.