Closely related species with parapatric elevational ranges are ubiquitous in tropical mountains worldwide. The gradient speciation hypothesis proposes that these series are the result of in situ ecological speciation driven by divergent selection across elevation. Direct tests of this scenario have been hampered by the difficulty inferring the geographic arrangement of populations at the time of divergence. In cichlids, sticklebacks and
Accelerating climate change and habitat loss make it imperative that plans to conserve biodiversity consider species' ability to adapt to changing environments. However, in biomes where biodiversity is highest, the evolutionary mechanisms responsible for generating adaptative variation and, ultimately, new species are frequently poorly understood. African rainforests represent one such biome, as decadal debates continue concerning the mechanisms generating African rainforest biodiversity. These debates hinge on the relative importance of geographic isolation versus divergent natural selection across environmental gradients. Hindering progress is a lack of robust tests of these competing hypotheses. Because African rainforests are severely at‐risk due to climate change and other anthropogenic activities, addressing this long‐standing debate is critical for making informed conservation decisions. We use demographic inference and allele frequency‐environment relationships to investigate mechanisms of diversification in an African rainforest skink,
- NSF-PAR ID:
- 10408606
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 32
- Issue:
- 9
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 2287-2300
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Timema stick insects, support for ecological speciation driven by other selective pressures has come from demonstrating parallel speciation, where divergence proceeds independently across replicated environmental gradients. Here, we take advantage of the unique geography of the island of New Guinea to test for parallel gradient speciation in replicated populations ofSyma kingfishers that show extremely subtle differentiation across elevation and between historically isolated mountain ranges. We find that currently described high‐elevation and low‐elevation species have reciprocally monophyletic gene trees and form nuclear DNA clusters, rejecting this hypothesis. However, demographic modelling suggests selection has likely maintained species boundaries in the face of gene flow following secondary contact. We compile evidence from the published literature to show that although in situ gradient speciation in labile organisms such as birds appears rare, divergent selection and post‐speciation gene flow may be an underappreciated force in the origin of elevational series and tropical beta diversity along mountain slopes. -
Abstract In ecological speciation, incipient species diverge due to natural selection that is ecologically based. In flowering plants, different pollinators could mediate that selection (pollinator-mediated divergent selection) or other features of the environment that differ between habitats of 2 species could do so (environment-mediated divergent selection). Although these mechanisms are well understood, they have received little rigorous testing, as few studies of divergent selection across sites of closely related species include both floral traits that influence pollination and vegetative traits that influence survival. This study employed common gardens in sites of the 2 parental species and a hybrid site, each containing advanced generation hybrids along with the parental species, to test these forms of ecological speciation in plants of the genus Ipomopsis. A total of 3 vegetative traits (specific leaf area, leaf trichomes, and photosynthetic water-use efficiency) and 5 floral traits (corolla length and width, anther insertion, petal color, and nectar production) were analyzed for impacts on fitness components (survival to flowering and seeds per flower, respectively). These traits exhibited strong clines across the elevational gradient in the hybrid zone, with narrower clines in theory reflecting stronger selection or higher genetic variance. Plants with long corollas and inserted anthers had higher seeds per flower at the Ipomopsis tenuituba site, whereas selection favored the reverse condition at the Ipomopsis aggregata site, a signature of divergent selection. In contrast, no divergent selection due to variation in survival was detected on any vegetative trait. Selection within the hybrid zone most closely resembled selection within the I. aggregata site. Across traits, the strength of divergent selection was not significantly correlated with width of the cline, which was better predicted by evolvability (standardized genetic variance). These results support the role of pollinator-mediated divergent selection in ecological speciation and illustrate the importance of genetic variance in determining divergence across hybrid zones.
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Abstract Selection along environmental gradients can drive reproductive isolation and speciation. Among fishes, salinity is a major factor limiting species distributions, and despite its importance in generating species diversity, speciation events between marine and freshwater are rare. Here, we tested for mechanisms of reproductive isolation between locally adapted freshwater and brackish water‐native populations of killifish,
Fundulus heteroclitus , from either side of a hybrid zone along a salinity gradient. There was evidence for pre‐zygotic endogenous reproductive isolation with reduced fertilization success between crosses of freshwater‐native males and brackish water‐native females. Exogenous pre‐zygotic isolation was also present where females had highest fertilization in their native salinity. We used a replicated mass spawning design to test for mate choice in both brackish and fresh water. After genotyping 187 parents and 2523 offspring at 2347 SNPs across the genome, 85% of offspring were successfully assign to their parents. However, no reinforcing mate choice was observed. These results therefore demonstrate emerging, yet limited, reproductive isolation and incipient speciation across a marine to freshwater salinity gradient and suggest that both endogenous and exogenous mechanisms, but not assortative mating, contribute to divergence. -
Abstract Habitat-specific thermal responses are well documented in various organisms and likely determine the vulnerability of populations to climate change. However, the underlying roles of genetics and plasticity that shape such habitat-specific patterns are rarely investigated together. Here we examined the thermal plasticity of the butterfly Bicyclus dorothea originating from rainforest and ecotone habitats in Cameroon under common garden conditions. We also sampled wild-caught butterflies from forest and ecotone sites and used RADseq to explore genome-wide population differentiation. We found differences in the level of phenotypic plasticity across habitats. Specifically, ecotone populations exhibited greater sensitivity in wing eyespot features with variable development temperatures relative to rainforest populations. Known adaptive roles of wing eyespots in Bicyclus species suggest that this morphological plasticity is likely under divergent selection across environmental gradients. However, we found no distinct population structure of genome-wide variation between habitats, suggesting high level of ongoing gene flow between habitats is homogenizing most parts of the genome.
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Abstract Context Processes that shape genomic and ecological divergence can reveal important evolutionary dynamics to inform the conservation of threatened species.
Fontainea is a genus of rainforest shrubs and small trees including critically endangered and threatened species restricted to narrow, but complex geographic and ecological regions. Several species ofFontainea are subject to spatially explicit conditions and experience limited intra-specific gene flow, likely generating genetic differentiation and local adaptation.Objectives Here, we explored the genetic and ecological mechanisms underlying patterns of diversification in two, closely related threatened
Fontainea species. Our aim was to compare spatial patterns of genetic variation between the vulnerableFontainea australis (Southern Fontainea) and critically endangeredF. oraria (Coastal Fontainea), endemic to the heterogeneous subtropical region of central, eastern Australia, where large-scale clearing has severely reduced rainforest habitat to a fraction (< 1%) of its pre-European settlement extent.Methods We used a set of 10,000 reduced-representation markers to infer genetic relationships and the drivers of spatial genetic variation across the two species. In addition, we employed a combination of univariate and multivariate genome-environment association analysis using a set of topo-climatic variables to explore potential patterns of local adaptation as a factor impacting genomic divergence.
Results Our study revealed that Coastal Fontainea have a close genetic relationship with Southern Fontainea. We showed that isolation by distance has played a key role in their genetic variation, indicating that vicariance can explain the spatial genetic distribution of the two species. Genotype-environment analyses showed a strong association with temperature and topographic features, suggesting adaptation to localised thermal environments. We used a multivariate redundancy analysis to identify a range of putatively adapted loci associated with local environmental conditions.
Conclusions Divergent selection at the local-habitat scale as a result of dispersal limitations and environmental heterogeneity (including physical barriers) are likely contributors to adaptive divergence between the two
Fontainea species. Our findings have presented evidence to indicate that Southern and Coastal Fontainea were comprised of distinct genetic groups and ecotypes, that together may form a single species continuum, with further phenotype research suggested to confirm the current species boundaries. Proactive conservation actions, including assisted migration to enhance the resilience of populations lacking stress-tolerant single nucleotide polymorphisms (SNPs) may be required to secure the long-term future of both taxa. This is especially vital for the critically endangered Coastal Fontainea given projections of habitat decline for the species under future climate scenarios.