Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structure (original) (raw)

Against all odds: a tale of marine range expansion with maintenance of extremely high genetic diversity

Nature research Scientific Reports, 2020

the displacement of species from equatorial latitudes to temperate locations following the increase in sea surface temperatures is among the significant reported consequences of climate change. Shifts in the distributional ranges of species result in fish communities tropicalisation, i.e., high latitude colonisations by typically low latitude distribution species. these movements create new interactions between species and new trophic assemblages. the Senegal seabream, Diplodus bellottii, may be used as a model to understand the population genetics of these invasions. in the last decades, this species has undergone an outstanding range expansion from its African area of origin to the Atlantic coast of the iberian peninsula, where now occurs abundantly. Mitochondrial and nuclear markers revealed a striking high haplotypic nucleotide and genetic diversity values, along with significant population differentiation throughout the present-day geographical range of the Senegal seabream. These results are not consistent with the central-marginal hypothesis, nor with the expectations of a leptokurtic distribution of individuals, as D. bellottii seems to be able to retain exceptional levels of diversity in marginal and recently colonised areas. We discuss possible causes for hyperdiversity and lack of geographical structure and subsequent implications for fisheries. Tropicalisation, the displacement of species from equatorial latitudes to temperate locations, is one of the major reported consequences of climate changes 1-3. The increase of sea surface temperatures (SSTs) in the last decades has promoted shifts in the distributional ranges of species (e.g., 4,5) with individuals moving into areas best corresponding to their physiological optimum. Additionally, the ability of a species to colonise new habitats is influenced by oceanographic currents, the existence of adequate resource availability (i.e., habitat and food) and life-history patterns (e.g., number of eggs produced, age or parental care). These movements lead to the colonization of more poleward habitats by low latitude species, and create new interactions between species and new trophic assemblages. In commercial species, these shifts due to climate change can be magnified by fishing pressures, as reported for the North Sea cod (e.g., 6). Poleward colonization by organisms with a typically equatorial distribution was described almost three decades ago for terrestrial organisms in association with postglacial recolonisation routes (e.g., 7-10). As a general rule, organisms follow a leptokurtic distribution type, in which the majority of individuals stay at or near the original area, and only a fraction disperse to longer distances. This range extension is usually done in a steppingstone manner, implying that each settlement has fewer individuals compared with the previous one. Theoretically, this process corresponds to multiple successive genetic founder events associated with the corresponding genetic implications of the downsize in the effective population numbers: the erosion of the genetic diversity by genetic drift induces allele loss, the "southern richness and northern purity" paradigm 11. Additionally, the "central-marginal hypothesis" 12 posits that populations at the centre of the distribution have higher population sizes and gene flow, and peripheral (leading edge) populations, are smaller in size, have lower genetic diversity and will be more genetically differentiated 12. Phylogeographic studies using mitochondrial and nuclear genes revealed that species with similar environmental requirements and life-history traits often present distinct genetic and demographic historical patterns 13,14 .

ECOLOGICAL GENETICS IN THE NORTH ATLANTIC: ENVIRONMENTAL GRADIENTS AND ADAPTATION AT SPECIFIC LOCI

Ecology, 2008

The North Atlantic intertidal community provides a rich set of organismal and environmental material for the study of ecological genetics. Clearly defined environmental gradients exist at multiple spatial scales: there are broad latitudinal trends in temperature, meso-scale changes in salinity along estuaries, and smaller scale gradients in desiccation and temperature spanning the intertidal range. The geology and geography of the American and European coasts provide natural replication of these gradients, allowing for population genetic analyses of parallel adaptation to environmental stress and heterogeneity. Statistical methods have been developed that provide genomic neutrality tests of population differentiation and aid in the process of candidate gene identification. In this paper, we review studies of marine organisms that illustrate associations between an environmental gradient and specific genetic markers. Such highly differentiated markers become candidate genes for adaptation to the environmental factors in question, but the functional significance of genetic variants must be comprehensively evaluated. We present a set of predictions about locus-specific selection across latitudinal, estuarine, and intertidal gradients that are likely to exist in the North Atlantic. We further present new data and analyses that support and contradict these simple selection models. Some taxa show pronounced clinal variation at certain loci against a background of mild clinal variation at many loci. These cases illustrate the procedures necessary for distinguishing selection driven by internal genomic vs. external environmental factors. We suggest that the North Atlantic intertidal community provides a model system for identifying genes that matter in ecology due to the clarity of the environmental stresses and an extensive experimental literature on ecological function. While these organisms are typically poor genetic and genomic models, advances in comparative genomics have provided access to molecular tools that can now be applied to taxa with well-defined ecologies. As many of the organisms we discuss have tight physiological limits driven by climatic factors, this synthesis of molecular population genetics with marine ecology could provide a sensitive means of assessing evolutionary responses to climate change.

Spatial scale and divergent patterns of variation in adapted traits in the ocean

Ecology Letters, 2012

The geography of adaptive genetic variation is crucial to species conservation yet poorly understood in marine systems. We analyse the spatial scale of genetic variation in traits that broadly display adaptation throughout the range of a highly dispersive marine species. We conducted common garden experiments on the Atlantic silverside, Menidia menidia, from 39 locations along its 3 000 km range thereby mapping genetic variation for growth rate, vertebral number and sex determination. Each trait displayed unique clinal patterns, with significant differences (adaptive or not) occurring over very small distances. Breakpoints in the cline differed among traits, corresponding only partially with presumed eco-geographical boundaries. Because clinal patterns are unique to each selected character, neutral genes or those coding for a single character cannot serve as proxies for the genetic structure as a whole. Conservation plans designed to protect essential genetic subunits of a species will need to account for such complex spatial structures.

Locally adapted fish populations maintain small-scale genetic differentiation despite perturbation by a catastrophic flood event

BMC Evolutionary Biology, 2010

Background: Local adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and hence, lead to speciation. Perturbations by catastrophic events, however, can distort such parapatric ecological speciation processes. Here, we asked whether an exceptionally strong flood led to homogenization of gene pools among locally adapted populations of the Atlantic molly (Poecilia mexicana, Poeciliidae) in the Cueva del Azufre system in southern Mexico, where two strong environmental selection factors (darkness within caves and/or presence of toxic H 2 S in sulfidic springs) drive the diversification of P. mexicana. Nine nuclear microsatellites as well as heritable female life history traits (both as a proxy for quantitative genetics and for trait divergence) were used as markers to compare genetic differentiation, genetic diversity, and especially population mixing (immigration and emigration) before and after the flood.

Speciation in spatially structured populations : identifying genes responsible for local adaptation

2012

The determination of the genetic basis of adaptive traits in natural populations is fundamental to better understand how populations adaptively diverge in heterogeneous environments and eventually give rise to new species. This work describes the efforts to identify candidate loci influenced by selection in ocellated lizards (Lacerta lepida) along an environmental gradient in the Iberian Peninsula, strongly affected by climatic variables. Two subspecies are recognized at the opposite extremes of the gradient, L. l. iberica in the northwest and L. l. nevadensis in the southeast, with morphological differences that suggest their local adaptation. Candidate loci were detected through an AFLP genome scan. Detection of candidate loci with a frequentist method and with Bayesian method resulted in a similar proportion of outliers (3-4%), but only a few loci were detected by both methods, denoting differences in methods' sensitivity. Several outliers were associated with variation in temperature, insolation or precipitation along the gradient, suggesting the importance of these variables as selective pressures for local adaptation. Seven outliers were successfully characterized, being noncoding, with internal indels or repetitive elements as causes of length polymorphism, indicating that they might act as regulatory elements or are in linkage with the actual target of selection. The analysis of Mc1r, a candidate gene for coloration, revealed a nonconserved and derived substitution (T162I) associated with the brownish colour phenotype of L. l. nevadensis, suggesting a putative partial loss of function. Another substitution (S172C) was associated with the presence of black scales in both L. l. lepida and L. l. iberica, but no mutations were associated with the higher melanization of L. l. iberica. Analysis of genetic structure showed that L. l. nevadensis divergence is well supported by both neutral and non-neutral loci, confirming that the subspecies is at the final stages of its speciation process. L. l. iberica divergence from the nominal subspecies is mostly explained by a few adaptive loci, indicating that L. l. iberica might be at the early stages of ecological speciation.

Genomic architecture of parallel ecological divergence: beyond a single environmental contrast

2018

The genetic basis of parallel ecological divergence provides important clues to the operation of natural selection and the predictability of evolution. Many examples exist where binary environmental contrasts seem to drive parallel divergence. However, this simplified view can conceal important components of parallel divergence because environmental variation is often more complex. Here, we disentangle the genetic basis of parallel divergence across two axes of environmental differentiation (crab-predation vs. wave-action and low-shore vs. high-shore habitat contrasts) in the marine snail Littorina saxatilis, a well established natural system of parallel ecological divergence. We used whole-genome resequencing across multiple instances of these two environmental axes, at local and regional scales from Spain to Sweden. Overall, sharing of genetic differentiation is generally low but it is highly heterogeneous across the genome and increases at smaller spatial scales. We identified ge...

Identifying environmental correlates of intraspecific genetic variation

Heredity, 2016

Genetic variation is critical to the persistence of populations and their capacity to adapt to environmental change. The distribution of genetic variation across a species' range can reveal critical information that is not necessarily represented in species occurrence or abundance patterns. We identified environmental factors associated with the amount of intraspecific, individual-based genetic variation across the range of a widespread freshwater fish species, the Murray cod Maccullochella peelii. We used two different approaches to statistically quantify the relative importance of predictor variables, allowing for nonlinear relationships: a random forest model and a Bayesian approach. The latter also accounted for population history. Both approaches identified associations between homozygosity by locus and both disturbance to the natural flow regime and mean annual flow. Homozygosity by locus was negatively associated with disturbance to the natural flow regime, suggesting that river reaches with more disturbed flow regimes may support larger, more genetically diverse populations. Our findings are consistent with the hypothesis that artificially induced perennial flows in regulated channels may provide greater and more consistent habitat and reduce the frequency of population bottlenecks that can occur frequently under the highly variable and unpredictable natural flow regime of the system. Although extensive river regulation across eastern Australia has not had an overall positive effect on Murray cod numbers over the past century, regulation may not represent the primary threat to Murray cod survival. Instead, pressures other than flow regulation may be more critical to the persistence of Murray cod (for example, reduced frequency of large floods, overfishing and chemical pollution).