Phenotypic and genomic diversification with isolation by environment along elevational gradients in a neotropical treefrog

Abstract

Understanding how geographic and environmental heterogeneity drive local patterns of genetic variation is a major goal of ecological genomics and a key question in evolutionary biology. The tropical Andes and inter‐Andean valleys are shaped by markedly heterogeneous landscapes, where species experience strong selective processes. We examined genome‐wide SNP data together with behavioural and ecological traits (mating calls and body size) known to contribute to genetic isolation in anurans in the banana tree‐dwelling frog, Boana platanera, distributed across an environmental gradient in Central Colombia (northern South America). Here, we analysed the relationships between environmentally (temperature and precipitation) associated genetic and phenotypic differentiation and the potential drivers of isolation by environment along an elevation gradient. We identified candidate SNPs associated with temperature and body size, which follow a clinal pattern of genome‐wide differentiation tightly coupled with phenotypic variation: as elevation increases, B. platanera exhibits larger body size and longer call duration with more pulses but lower pulse rate and frequency. Thus, the environmental landscape has rendered a scenario where isolation by environment and candidate loci show concordance with phenotypic divergence in this tropical frog along an elevation gradient in the Colombian Andes. Our study sets the basis for evaluating the role of temperature in the genetic structure and local adaptation in tropical treefrogs and its putative effect on life cycle (embryos, tadpoles, adults) along elevation gradients.

Sexual imprinting leads to speciation in locally adapted populations

“…These studies demonstrate the potential for genome sequencing to investigate cases of incipient or complete parapatric speciation. If speciation followed the route described here then the loci differentiating two species would be expected to be of two types: (1) genes conferring habitat‐specific adaptions, as in de Leon et al (2010), Graham et al (2018), Hahn et al (2017), Han et al (2017), Hendry et al (2009), Medina et al (2021) and Orkin et al (2021); (2) genes responsible for the traits used in mate choice, such as plumage color and pattern, as in Toews et al (2016), or song.…”

“…Several locally adaptive genes, with F ST values in the range 0.44–0.77, were identified and their functions established. Islands of high divergence, within a genome‐wide background of low divergence, have also been reported in species of Darwin's finches differing in beak size and shape (Han et al, 2017), in four species of Lake Malawi cichlids varying in their adaptations to deepwater environments (Hahn et al, 2017), in two East Asian plovers (Wang et al, 2019) two North American parulid warblers (Toews et al, 2016), three species of sympatric snowfinch (She et al, 2021), within capuchin monkeys comparing those from tropical dry forests with those from lowland rain forest (Orkin et al, 2021), and within treefrogs Boana platanera in habitats varying from warm lowland valleys to cooler moist upland forest in the Andes (Medina et al, 2021). These studies demonstrate the potential for genome sequencing to investigate cases of incipient or complete parapatric speciation.…”

“…(1) genes conferring habitatspecific adaptions, as in deLeon et al (2010),Graham et al (2018),Hahn et al (2017),Han et al (2017),Hendry et al (2009), Medina et al (2021 andOrkin et al (2021); (2) genes responsible for the traits used in mate choice, such as plumage color and pattern, as inToews et al (2016), or song.Our results show that given sexual imprinting and local adaptation, a mutation giving males a new mating cue such as a new plumage colour can rapidly spread through a population and in so doing lead to speciation. This could explain some of the diversity of plumage colours seen in birds and cichlids, for example.…”

Temperature is a cryptic factor to shape the geographical pattern of genetic variation in Ceratophyllum demersum across a subtropical freshwater lake

“…Temperature-imposed selection usually leads to species local adaption across large geographic scale, where gradients of temperature often results in the spatial divergent thereby leads to the population divergence (Medina et al, 2021). Moreover, populations throughout the thermal regime exhibit different level of genetic diversity can confer benefits to the consumers, which further influence their genetic diversity and help to shape the population structure in return (Ruff et al, 2011;Farleigh et al, 2021).…”

Axes of multivariate sexual signal divergence among incipient species: Concordance with selection, genetic variation and phenotypic plasticity

“…Under a plasticity-first model, populations need not occupy habitats with persistent or dramatically distinct temperatures; relatively small or fluctuating thermal shifts might be adequate to promote initial phenotypic divergence if sufficiently isolated from one another. Like other tropical montane ecosystems, the mid-elevation Hawaiian rainforests in which L. cerasina occur are characterized by pronounced thermal stratification that has been hypothesized to promote diversification due to thermal adaptation in other arthropods (Polato et al, 2018;Tregenza et al, 2021) and vertebrates (Medina et al, 2021). Moreover, evidence suggests that cyclical patterns of habitat fragmentation due to volcanic activity have been an important driver of rapid character state evolution and population divergence in Hawaiian arthropods (Carson et al, 1990;Carson & Templeton, 1984;Vandergast et al, 2004).…”