How to Investigate the Origins of Novelty: Insights Gained from Genetic, Behavioral, and Fitness Perspectives

Martin, Christopher H.; McGirr, Joseph A.; Richards, Emilie J.; John, Michelle

doi:10.1093/iob/obz018

Cited by 17 publications

(20 citation statements)

References 187 publications

(141 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Overall, our results highlight the utility of the San Salvador Island pupfish system as an evolutionary mutant model for natural and clinical variation in human craniofacial phenotypes. Similar rapid speciation replicated across many environments can be found in other adaptive radiations ( Martin et al. 2019 ; Martin and Richards 2019 ; Levin et al.…”

Section: Discussionsupporting

confidence: 71%

Few Fixed Variants between Trophic Specialist Pupfish Species Reveal CandidateCis-Regulatory Alleles Underlying Rapid Craniofacial Divergence

McGirr

Martin

2020

Molecular Biology and Evolution

Self Cite

View full text Add to dashboard Cite

Investigating closely related species that rapidly evolved divergent feeding morphology is a powerful approach to identify genetic variation underlying variation in complex traits. This can also lead to the discovery of novel candidate genes influencing natural and clinical variation in human craniofacial phenotypes. We combined whole-genome resequencing of 258 individuals with 50 transcriptomes to identify candidate cis-acting genetic variation underlying rapidly evolving craniofacial phenotypes within an adaptive radiation of Cyprinodon pupfishes. This radiation consists of a dietary generalist species and two derived trophic niche specialists – a molluscivore and a scale-eating species. Despite extensive morphological divergence, these species only diverged 10 kya and produce fertile hybrids in the laboratory. Out of 9.3 million genome-wide SNPs and 80,012 structural variants, we found very few alleles fixed between species – only 157 SNPs and 87 deletions. Comparing gene expression across 38 purebred F1 offspring sampled at three early developmental stages, we identified 17 fixed variants within 10 kilobases of 12 genes that were highly differentially expressed between species. By measuring allele-specific expression in F1 hybrids from multiple crosses, we found that the majority of expression divergence between species was explained by trans-regulatory mechanisms. We also found strong evidence for two cis-regulatory alleles affecting expression divergence of two genes with putative effects on skeletal development (dync2li1 and pycr3). These results suggest that SNPs and structural variants contribute to the evolution of novel traits and highlight the utility of the San Salvador Island pupfish system as an evolutionary model for craniofacial development.

show abstract

Section: Discussionsupporting

confidence: 71%

Few Fixed Variants between Trophic Specialist Pupfish Species Reveal CandidateCis-Regulatory Alleles Underlying Rapid Craniofacial Divergence

McGirr

Martin

2020

Molecular Biology and Evolution

Self Cite

View full text Add to dashboard Cite

show abstract

“…The processes and underlying conditions that give rise to evolutionary novelties are incompletely understood [32]. Although evolutionary novelties can arise from the emergence of new ecological opportunities [33], this is not always the case [34].…”

Section: Origins Of a Novel Traitmentioning

confidence: 99%

“…For example, complex behaviours can be achieved through the integration of simpler, pre-existing behavioural modules [37]. However, the relative importance of behaviour, morphology and physiology as the ultimate drivers of novelty is debated [32]. Understanding fitness benefits during intermediate stages, and the timing of trait acquisition, is therefore key to disentangling the origins of an innovation.…”

Section: Origins Of a Novel Traitmentioning

confidence: 99%

Pollen feeding inHeliconiusbutterflies: the singular evolution of an adaptive suite

Young

Montgomery

2020

Proc. R. Soc. B.

View full text Add to dashboard Cite

Major evolutionary transitions can be triggered by behavioural novelty, and are often associated with ‘adaptive suites’, which involve shifts in multiple co-adapted traits subject to complex interactions. Heliconius butterflies represent one such example, actively feeding on pollen, a behaviour unique among butterflies. Pollen feeding permits a prolonged reproductive lifespan, and co-occurs with a constellation of behavioural, neuroanatomical, life history, morphological and physiological traits that are absent in closely related, non-pollen-feeding genera. As a highly tractable system, supported by considerable ecological and genomic data, Heliconius are an excellent model for investigating how behavioural innovation can trigger a cascade of adaptive shifts in multiple diverse, but interrelated, traits. Here, we synthesize current knowledge of pollen feeding in Heliconius , and explore potential interactions between associated, putatively adaptive, traits. Currently, no physiological, morphological or molecular innovation has been explicitly linked to the origin of pollen feeding, and several hypothesized links between different aspects of Heliconius biology remain poorly tested. However, resolving these uncertainties will contribute to our understanding of how behavioural innovations evolve and subsequently alter the evolutionary trajectories of diverse traits impacting resource acquisition, life history, senescence and cognition.

show abstract

“…Evolutionary novelties and innovations are often seen as rare, or at least uncommon (Martin et al ., 2019). Indeed some, such as the novelties associated with the origin of eukaryotes may have been unique.…”

Section: Current and Past Views Of Evolutionary Novelty And Innovationmentioning

confidence: 99%

A conceptual framework of evolutionary novelty and innovation

Erwin

2020

Biological Reviews

View full text Add to dashboard Cite

Since 1990 the recognition of deep homologies among metazoan developmental processes and the spread of more mechanistic approaches to developmental biology have led to a resurgence of interest in evolutionary novelty and innovation. Other evolutionary biologists have proposed central roles for behaviour and phenotypic plasticity in generating the conditions for the construction of novel morphologies, or invoked the accessibility of new regions of vast sequence spaces. These approaches contrast with more traditional emphasis on the exploitation of ecological opportunities as the primary source of novelty. This definitional cornucopia reflects differing stress placed on three attributes of novelties: their radical nature, the generation of new taxa, and ecological and evolutionary impact. Such different emphasis has led to conflating four distinct issues: the origin of novel attributes (genes, developmental processes, phenotypic characters), new functions, higher clades and the ecological impact of new structures and functions. Here I distinguish novelty (the origin of new characters, deep character transformations, or new combinations) from innovation, the ecological and evolutionary success of clades. Evidence from the fossil record of macroevolutionary lags between the origin of a novelty and its ecological success demonstrates that novelty may be decoupled from innovation, and only definitions of novelty based on radicality (rather than generativity or consequentiality) can be assessed without reference to the subsequent history of the clade to which a novelty belongs. These considerations suggest a conceptual framework for novelty and innovation, involving: (i) generation of the potential for novelty; (ii) the formation of novel attributes; (iii) refinement of novelties through adaptation; (iv) exploitation of novelties by a clade, which may coincide with a new round of ecological or environmental potentiation; followed by (v) the establishment of innovations through ecological processes. This framework recognizes that there is little empirical support for either the dominance of ecological opportunity, nor abrupt discontinuities (often caricatured as ‘hopeful monsters’). This general framework may be extended to aspects of cultural and social innovation.

show abstract

How to Investigate the Origins of Novelty: Insights Gained from Genetic, Behavioral, and Fitness Perspectives

Cited by 17 publications

References 187 publications

Few Fixed Variants between Trophic Specialist Pupfish Species Reveal CandidateCis-Regulatory Alleles Underlying Rapid Craniofacial Divergence

Few Fixed Variants between Trophic Specialist Pupfish Species Reveal CandidateCis-Regulatory Alleles Underlying Rapid Craniofacial Divergence

Pollen feeding inHeliconiusbutterflies: the singular evolution of an adaptive suite

A conceptual framework of evolutionary novelty and innovation

Contact Info

Product

Resources

About