Recurrent adaptation in a low-dispersal trait

The study of natural populations from contrasting environments has greatly enhanced our understanding of ecological-dependent selection, adaptation and speciation. Cases of parallel evolution in particular have facilitated the study of the molecular and genetic basis of adaptive variation. This includes the type and number of genes underlying adaptive traits, as well as the extent to which these genes are exchanged among populations and contribute repeatedly to parallel evolution. Yet, surprisingly few studies provide a comprehensive view on the evolutionary history of adaptive traits from mutation to widespread adaptation. When did key mutations arise, how did they increase in frequency, and how did they spread? In this issue of Molecular Ecology, Van Belleghem et al. () reconstruct the evolutionary history of a gene associated with wing size in the salt marsh beetle Pogonus chalceus. Screening the entire distribution range of this species, they found a single origin for the allele associated with the short-winged ecotype. This allele seemingly evolved in an isolated population and rapidly introgressed into other populations. These findings suggest that the adaptive genetic variation found in sympatric short- and long-winged populations has an allopatric origin, confirming that allopatric phases may be important at early stages of speciation

Adaptive and non-adaptive divergence in a common landscape

Species in a common landscape often face similar selective environments. The capacity of organisms to adapt to these environments may be largely species specific. Quantifying shared and unique adaptive responses across species within landscapes may thus improve our understanding of landscape-moderated biodiversity patterns. Here we test to what extent populations of two coexisting and phylogenetically related fishes—three-spined and nine-spined stickleback—differ in the strength and nature of neutral and adaptive divergence along a salinity gradient. Phenotypic differentiation, neutral genetic differentiation and genomic signatures of adaptation are stronger in the three-spined stickleback. Yet, both species show substantial phenotypic parallelism. In contrast, genomic signatures of adaptation involve different genomic regions, and are thus non-parallel. The relative contribution of spatial and environmental drivers of population divergence in each species reflects different strategies for persistence in the same landscape. These results provide insight in the mechanisms underlying variation in evolutionary versatility and ecological success among species within landscapes

Spatial and seasonal variation in reproductive indices of the clupeids Limnothrissa miodon and Stolothrissa tanganicae in the Congolese waters of northern Lake Tanganyika

peer reviewedKnowledge on the reproductive biology of the endemic clupeids Limnothrissa miodon and Stolothrissa tanganicae, two main target species of the pelagic fisheries of Lake Tanganyika, is constrained by fragmented monitoring activities. Here, we investigate the nursing areas of L. miodon, the timing of reproductive activities of littoral and pelagic L. miodon, and the timing of reproductive activities of pelagic S. tanganicae in the Congolese waters of the northern end of Lake Tanganyika (Bujumbura sub-basin). Nursing areas were determined year-round (2009–2010) based on the presence of clupeid larvae at two sandy and two stony beaches. The gonadosomatic index (GSI) and the proportion of fish having ripe gonads were used to study variation in reproductive indices in space (littoral vs. pelagic zones) during one year (2013–2014), as well as in time (dry vs. rainy season) during three years (2013–2016). Larvae of L. miodon were more frequently encountered on sandy than on stony beaches. Mature L. miodon females were more abundant in the littoral than in the pelagic zone, while the proportion of mature males in both habitats was similar. Irregular, low amplitude peaks could be distinguished in the GSI and proportion of mature males and females, but averages only differed between the dry and the rainy season in males. In contrast, GSI and proportions of mature males and females in S. tanganicae were higher in the dry season than in the rainy season. The reproductive effort of males and females of S. tanganicae and littoral L. miodon, but not pelagic L. miodon, was strongly synchronized. Interestingly, reproductive investment was also synchronised between pelagic male L. miodon, and pelagic S. tanganicae. Our time series strongly supports the view that L. miodon reproduces year-round in the littoral zone, while reproduction in S. tanganicae is seasonal. For fisheries management, we recommend year-round protection of sandy beaches, which are the main breeding grounds for L. miodon. © 2022, Royal Belgian Institute of Natural Sciences. All rights reserved

Infection dynamics of the monogenean parasite <i>Gyrodactylus gasterostei</i> on sympatric and allopatric populations of the three-spined stickleback <i>Gasterosteus aculeatus</i>

Parasites with high host specificity maximally depend on their hosts, which should increase the likelihood of coevolution. However, coevolution requires reciprocal selection exerted by the host and the parasite, and thus a considerable level of parasite virulence. In species of the monogenean ectoparasite genus Gyrodactylus consecutive generations are confronted with a single host, which may constrain the evolution of virulence. Transmission, which is often important in the ecology of Gyrodactylus species, may have the opposite effect, but may also lead to the avoidance of coevolutionary arms races. We investigated the potential outcome of coevolution between Gyrodactylus gasterostei Gläser, 1974 and its host, the three-spined stickleback (Gasterosteus aculeatus L.) by determining the strength of genotype by genotype (G×G) interactions on two levels: within and between sympatric and allopatric host populations. To do so, we compared the parasite’s infection dynamics on laboratory-reared sympatric (Belgian) and allopatric (German) hosts. We found that a parasite line successfully infected a range of sympatric host genotypes (represented by families), while it failed to establish on allopatric hosts. Phylogeographic studies suggest that neutral genetic divergence between the host populations cannot explain this dramatic difference. Provided that this result can be generalised towards other parasite lines, we conclude that coevolution in this host-parasite system is more likely to lead to local adaptation on the population level than to G×G interactions within populations

Detecting Holocene divergence in the anadromous-freshwater three-spined stickleback (<i>Gasterosteus aculeatus</i>) system

The anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system allows for inferring the role of adaptation in speciation with a high level of accuracy because the freshwater ecotype has evolved multiple times from a uniform anadromous ancestor. A cause for concern is that independent evolution among drainages is not guaranteed in areas with a poorly resolved glacial history. This is the case for the west European great rivers, whose downstream valleys flanked the southern limit of the late Pleistocene ice sheet. We tested for independent and postglacial colonization of these valleys hypothesizing that the relationships among anadromous and freshwater sticklebacks correspond to a raceme structure. We compared the reduction in plate number accompanying this colonization to the genetic differentiation using 13 allozyme and five microsatellite loci in 350 individuals. Overall microsatellite differentiation (FST = 0.147) was twice as large as allozyme differentiation (FST = 0.066). Although habitat-specific gene flow may mask the ancestral relationships among both ecotypes, levels of microsatellite differentiation supported the hypothesis of raceme-like divergence, reflecting independent colonizations rather than the presence of two distinct evolutionary clades. Under an infinite alleles model and in the absence of gene flow, the observed freshwater divergence might be reached after 440 (microsatellites) to 4500 (allozymes) generations. Hence, the anadromous-freshwater stickleback system most likely diverged postglacially. We conclude that the reduction in plate number in two freshwater basins probably occurred independently, and that its considerable variation among populations is not in agreement with the time since divergence

Community structure, population structure and topographical specialisation of <i>Gyrodactylus</i> (Monogenea) ectoparasites living on sympatric stickleback species

In order to disentangle the contribution of host and parasite biology to host specificity, we compared the structure and population dynamics of the Gyrodactylus (von Nordmann, 1832) flatworm community living on sympatric three-spined Gasterosteus aculeatus L. and nine-spined Pungitius pungitius (L.) stickleback. Between April 2002 and March 2003, a small lowland creek was sampled monthly. Species identity of about 75% of the worms per host was determined with a genetic nuclear marker (ITS1). Each stickleback species hosted a characteristic gill- and fin-parasitic Gyrodactylus: G. arcuatus Bychowsky, 1933 and G. gasterostei Gläser, 1974 respectively infecting the three-spined stickleback, with G. rarus Wegener, 1910 and G. pungitii Malmberg, 1964 infecting the nine-spined stickleback. Host size and seasonal dynamics were strong determinants of parasite abundance. A strong interaction between host and parasite species determined infection levels and affected three levels of parasite organisation: community structure, population structure and topographical specialisation. Community and population structure were shaped by asymmetric cross-infections, resulting in a net transmission of the Gyrodactylus species typical of the nine-spined stickleback towards the three-spined stickleback. Host density was not a major determinant of parasite exchange. Aggregation and topographical specialisation of the Gyrodactylus species of the three-spined stickleback were more pronounced than that of the nine-spined stickleback

Microsatellite conservation and Bayesian individual assignment in four Anguilla species

Microsatellite flanking regions are often highly conserved in fish taxa, enabling their application in other species within or outside the source family. Moderately variable microsatellite markers may also be good candidates for species identification using multi-locus genotypes. We evaluated the degree of conservation of microsatellite flanking regions and the level of polymorphism in 4 commercially important eel species (Anguilla anguilla, A. rostrata, A. japonica and A, marmorata). Using multiplex polymerase chain reactions developed for the first 2 taxa, we assessed the discrimination power of an individual-based assignment method to differentiate all 4 species without initial species information. Detection and classification of each species was performed with high confidence (> 90%), as was assignment of randomly sampled individuals to pre-defined species (> 95%). Our results demonstrate the highly conserved nature of microsatellites and their level of polymorphism in Anguilla species. Although an inverse relationship was found between genetic diversity and differentiation estimates, likely due to homoplasy, assignment proved to be superior to multivariate and distance-based approaches for identifying the 4 species. The method enables the rapid screening of morphologically similar eel species using only 4 co-dominant nuclear loci and the detection of natural hybridisation or anthropogenic mixing between internationally highly traded species