scholarly journals Adaptive divergence in shoot gravitropism creates intrinsic reproductive isolation in an Australian wildflower

2019 ◽  
Author(s):  
Melanie J. Wilkinson ◽  
Federico Roda ◽  
Greg M. Walter ◽  
Maddie E. James ◽  
Rick Nipper ◽  
...  

AbstractAdaptation to the local environment is a major driver of speciation. Yet, it remains largely unknown whether natural selection directly causes intrinsic reproductive isolation (hybrid sterility or inviability) between locally adapted populations. Here, we show that adaptive divergence in shoot gravitropism, the ability of a plant’s shoot to bend upwards in response to the downward pull of gravity, contributes to the evolution of intrinsic reproductive isolation in an Australian wildflower, Senecio lautus. We find that shoot gravitropism has evolved multiple times in association with plant height between adjacent populations inhabiting contrasting environments, suggesting that these traits have evolved by natural selection. We directly tested this prediction in multi-year reciprocal transplant experiments using hybrid populations. We show that shoot gravitropism and plant height respond to natural selection in the expected direction of the locally adapted population. Remarkably, we find that crossing F11 hybrid individuals with extreme differences in gravitropism significantly reduces their ability to produce seeds, providing strong evidence that this adaptive trait is genetically correlated with intrinsic reproductive isolation. Our results suggest that natural selection can drive the evolution of locally adaptive traits that incidentally create intrinsic reproductive isolation, thus increasing our understanding of the origin and maintenance of new species.

2021 ◽  
Vol 118 (47) ◽  
pp. e2004901118
Author(s):  
Melanie J. Wilkinson ◽  
Federico Roda ◽  
Greg M. Walter ◽  
Maddie E. James ◽  
Rick Nipper ◽  
...  

Natural selection is responsible for much of the diversity we see in nature. Just as it drives the evolution of new traits, it can also lead to new species. However, it is unclear whether natural selection conferring adaptation to local environments can drive speciation through the evolution of hybrid sterility between populations. Here, we show that adaptive divergence in shoot gravitropism, the ability of a plant’s shoot to bend upwards in response to the downward pull of gravity, contributes to the evolution of hybrid sterility in an Australian wildflower, Senecio lautus. We find that shoot gravitropism has evolved multiple times in association with plant height between adjacent populations inhabiting contrasting environments, suggesting that these traits have evolved by natural selection. We directly tested this prediction using a hybrid population subjected to eight rounds of recombination and three rounds of selection in the field. Our experiments revealed that shoot gravitropism responds to natural selection in the expected direction of the locally adapted population. Using the advanced hybrid population, we discovered that individuals with extreme differences in gravitropism had more sterile crosses than individuals with similar gravitropic responses, which were largely fertile, indicating that this adaptive trait is genetically correlated with hybrid sterility. Our results suggest that natural selection can drive the evolution of locally adaptive traits that also create hybrid sterility, thus revealing an evolutionary connection between local adaptation and the origin of new species.


2019 ◽  
Vol 116 (26) ◽  
pp. 12933-12941 ◽  
Author(s):  
David B. Lowry ◽  
John T. Lovell ◽  
Li Zhang ◽  
Jason Bonnette ◽  
Philip A. Fay ◽  
...  

Local adaptation is the process by which natural selection drives adaptive phenotypic divergence across environmental gradients. Theory suggests that local adaptation results from genetic trade-offs at individual genetic loci, where adaptation to one set of environmental conditions results in a cost to fitness in alternative environments. However, the degree to which there are costs associated with local adaptation is poorly understood because most of these experiments rely on two-site reciprocal transplant experiments. Here, we quantify the benefits and costs of locally adaptive loci across 17° of latitude in a four-grandparent outbred mapping population in outcrossing switchgrass (Panicum virgatumL.), an emerging biofuel crop and dominant tallgrass species. We conducted quantitative trait locus (QTL) mapping across 10 sites, ranging from Texas to South Dakota. This analysis revealed that beneficial biomass (fitness) QTL generally incur minimal costs when transplanted to other field sites distributed over a large climatic gradient over the 2 y of our study. Therefore, locally advantageous alleles could potentially be combined across multiple loci through breeding to create high-yielding regionally adapted cultivars.


2019 ◽  
Author(s):  
Joseph A. McGirr ◽  
Christopher H. Martin

AbstractEcological speciation occurs when reproductive isolation evolves as a byproduct of adaptive divergence between populations. However, it is unknown whether divergent ecological selection on gene regulation can directly cause reproductive isolation. Selection favoring regulatory divergence between species could result in gene misregulation in F1 hybrids and ultimately lower hybrid fitness. We combined 58 resequenced genomes with 124 transcriptomes to test this hypothesis in a young, sympatric radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas, which consists of a dietary generalist and two novel trophic specialists – a molluscivore and a scale-eater. We found more differential gene expression between closely related sympatric specialists than between allopatric generalist populations separated by 1000 km. Intriguingly, 9.6% of genes that were differentially expressed between sympatric species were also misregulated in their F1 hybrids. Consistent with divergent ecological selection causing misregulation, a subset of these genes were in highly differentiated genomic regions and enriched for functions important for trophic specialization, including head, muscle, and brain development. These regions also included genes that showed evidence of hard selective sweeps and were significantly associated with oral jaw length – the most rapidly diversifying skeletal trait in this radiation. Our results indicate that divergent ecological selection in sympatry can cause hybrid gene misregulation which may act as a primary reproductive barrier between nascent species.SignificanceIt is unknown whether the same genes that regulate ecological traits can simultaneously contribute to reproductive barriers between species. We measured gene expression in two trophic specialist species of Cyprinodon pupfishes that rapidly diverged from a generalist ancestor. We found genes differentially expressed between species that also showed extreme expression levels in their hybrid offspring. Many of these genes showed signs of selection and have putative effects on the development of traits that are important for ecological specialization. This suggests that genetic variants contributing to adaptive trait divergence between parental species negatively interact to cause hybrid gene misregulation, potentially producing unfit hybrids. Such loci may be important barriers to gene flow during the early stages of speciation, even in sympatry.


2002 ◽  
Vol 357 (1420) ◽  
pp. 471-492 ◽  
Author(s):  
Michele Drès ◽  
James Mallet

The existence of a continuous array of sympatric biotypes—from polymorphisms, through ecological or host races with increasing reproductive isolation, to good species—can provide strong evidence for a continuous route to sympatric speciation via natural selection. Host races in plant–feeding insects, in particular, have often been used as evidence for the probability of sympatric speciation. Here, we provide verifiable criteria to distinguish host races from other biotypes: in brief, host races are genetically differentiated, sympatric populations of parasites that use different hosts and between which there is appreciable gene flow. We recognize host races as kinds of species that regularly exchange genes with other species at a rate of more than ca . 1% per generation, rather than as fundamentally distinct taxa. Host races provide a convenient, although admittedly somewhat arbitrary intermediate stage along the speciation continuum. They are a heuristic device to aid in evaluating the probability of speciation by natural selection, particularly in sympatry. Speciation is thereby envisaged as having two phases: (i) the evolution of host races from within polymorphic, panmictic populations; and (ii) further reduction of gene flow between host races until the diverging populations can become generally accepted as species. We apply this criterion to 21 putative host race systems. Of these, only three are unambiguously classified as host races, but a further eight are strong candidates that merely lack accurate information on rates of hybridization or gene flow. Thus, over one–half of the cases that we review are probably or certainly host races, under our definition. Our review of the data favours the idea of sympatric speciation via host shift for three major reasons: (i) the evolution of assortative mating as a pleiotropic by–product of adaptation to a new host seems likely, even in cases where mating occurs away from the host; (ii) stable genetic differences in half of the cases attest to the power of natural selection to maintain multilocus polymorphisms with substantial linkage disequilibrium, in spite of probable gene flow; and (iii) this linkage disequilibrium should permit additional host adaptation, leading to further reproductive isolation via pleiotropy, and also provides conditions suitable for adaptive evolution of mate choice (reinforcement) to cause still further reductions in gene flow. Current data are too sparse to rule out a cryptic discontinuity in the apparently stable sympatric route from host–associated polymorphism to host–associated species, but such a hiatus seems unlikely on present evidence. Finally, we discuss applications of an understanding of host races in conservation and in managing adaptation by pests to control strategies, including those involving biological control or transgenic parasite–resistant plants.


1953 ◽  
Vol 85 (4) ◽  
pp. 141-151 ◽  
Author(s):  
Stanley G. Smith

According to Dobzhansky (1951a, p. 262) “Species are … groups of populations the gene exchange between which is limited or prevented by one, or by a combination of several, reproductive isolating mechanisms”. This definition follows from his concept of a species not as a static unit but as a stage in the process of evolutionary divergence. Limitation or prevention of gene exchange is a property of geographic and reproductive isolation (Mayr, 1912), the various types of which Dobzhansky lists as follows:I. Geographic or Spatial IsolationII. Reproductive IsolationA. Ecological IsolationB. Seasonal or Temporal IsolationC. Sexual, Psychological or Ethnological IsolationD. Mechanical IsolationE. Gametic IsolationF. Hybrid InviabilityG. Hybrid SterilityH. Hybrid Breakdown


Sign in / Sign up

Export Citation Format

Share Document