Speciation in caves: experimental evidence that permanent darkness promotes reproductive isolation

Divergent selection through biotic factors like predation or parasitism can promote reproductive isolation even in the absence of geographical barriers. On the other hand, evidence for a role of adaptation to abiotic factors during ecological speciation in animals is scant. In particular, the role played by perpetual darkness in establishing reproductive isolation in cave animals (troglobites) remains elusive. We focused on two reproductively isolated ecotypes (surface- and cave-dwelling) of the widespread livebearer Poecilia mexicana , and raised offspring of wild-caught females to sexual maturity in a 12-month common-garden experiment. Fish were reared in light or darkness combined with high- or low-food conditions. Females, but not males, of the surface ecotype suffered from almost complete reproductive failure in darkness, especially in the low-food treatment. Furthermore, surface fish suffered from a significantly higher rate of spontaneous, stress-related infection with bacterial columnaris disease. This experimental evidence for strong selection by permanent darkness on non-adapted surface-dwelling animals adds depth to our understanding of the selective forces establishing and maintaining reproductive isolation in cave faunas.

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Effects of early growth conditions on body composition, allometry, and survival in the ladybird beetle Harmonia axyridis

Canadian Journal of Zoology ◽

10.1139/z09-001 ◽

2009 ◽

Vol 87 (2) ◽

pp. 175-182 ◽

Cited By ~ 18

Author(s):

C. Dmitriew ◽

J. Carroll ◽

L. Rowe

Keyword(s):

Harmonia Axyridis ◽

Larval Growth ◽

Reproductive Traits ◽

Growth Conditions ◽

Adult Survival ◽

High Food ◽

Food Treatment ◽

Dispersal Traits ◽

Food Conditions ◽

Harmonia Axyridis Pallas

During both the larval and adult stages, the ladybird beetles Harmonia axyridis (Pallas, 1773) feed primarily on aphids, populations of which may fluctuate dramatically in time and space. Harmonia axyridis were reared under three resource treatments: high, low, and improving. We predicted that beetles experiencing consistently poor larval conditions would allocate limited resources to dispersal traits (by increasing relative wing surface area and fat storage), whereas larvae facing good or improving conditions were predicted to allocate preferentially to reproductive traits. As predicted, beetles reared at low food had lower wing loading and stored more fat than individuals reared at consistently high food. When conditions were initially poor but improved during development, body size was reduced relative to the high food treatment, though wing area scaled similarly. Allocation of fat and protein was dependent on both sex and treatment. Females in improving conditions stored less fat, and males less protein, relative to low food conditions. This is suggestive of a trade-off between reproduction and dispersal that is resolved differently between the sexes. Unexpectedly, adult survival under starvation was not appreciably affected by larval growth conditions, although males lived about 10 days longer, on average.

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Genome-wide patterns of divergence during speciation: the lake whitefish case study

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2011.0197 ◽

2012 ◽

Vol 367 (1587) ◽

pp. 354-363 ◽

Cited By ~ 81

Author(s):

S. Renaut ◽

N. Maillet ◽

E. Normandeau ◽

C. Sauvage ◽

N. Derome ◽

...

Keyword(s):

Reproductive Isolation ◽

Genomic Islands ◽

Next Generation Sequencing Data ◽

Adaptive Divergence ◽

Phenotypic Traits ◽

Lake Whitefish ◽

Sequencing Data ◽

Species Pairs ◽

Selective Forces ◽

Genomic Regions

The nature, size and distribution of the genomic regions underlying divergence and promoting reproductive isolation remain largely unknown. Here, we summarize ongoing efforts using young (12 000 yr BP) species pairs of lake whitefish ( Coregonus clupeaformis ) to expand our understanding of the initial genomic patterns of divergence observed during speciation. Our results confirmed the predictions that: (i) on average, phenotypic quantitative trait loci (pQTL) show higher F ST values and are more likely to be outliers (and therefore candidates for being targets of divergent selection) than non-pQTL markers; (ii) large islands of divergence rather than small independent regions under selection characterize the early stages of adaptive divergence of lake whitefish; and (iii) there is a general trend towards an increase in terms of numbers and size of genomic regions of divergence from the least (East L.) to the most differentiated species pair (Cliff L.). This is consistent with previous estimates of reproductive isolation between these species pairs being driven by the same selective forces responsible for environment specialization. Altogether, dwarf and normal whitefish species pairs represent a continuum of both morphological and genomic differentiation contributing to ecological speciation. Admittedly, much progress is still required to more finely map and circumscribe genomic islands of speciation. This will be achieved through the use of next generation sequencing data but also through a better quantification of phenotypic traits moulded by selection as organisms adapt to new environmental conditions.

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Limited phenological and pollinator-mediated isolation among selfing and outcrossing Arabidopsis lyrata populations

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.2323 ◽

2020 ◽

Vol 287 (1939) ◽

pp. 20202323

Author(s):

Courtney E. Gorman ◽

Lindsay Bond ◽

Mark van Kleunen ◽

Marcel E. Dorken ◽

Marc Stift

Keyword(s):

Reproductive Isolation ◽

Mating System ◽

Common Garden ◽

Common Garden Experiment ◽

Pollinator Visitation ◽

Arabidopsis Lyrata ◽

Pollinator Preference ◽

Pollination Mechanisms ◽

Self Fertilization ◽

Mechanistic Basis

Transitions from outcrossing to selfing have been a frequent evolutionary shift in plants and clearly play a role in species divergence. However, many questions remain about the initial mechanistic basis of reproductive isolation during the evolution of selfing. For instance, how important are pre-zygotic pre-pollination mechanisms (e.g. changes in phenology and pollinator visitation) in maintaining reproductive isolation between newly arisen selfing populations and their outcrossing ancestors? To test whether changes in phenology and pollinator visitation isolate selfing populations of Arabidopsis lyrata from outcrossing populations, we conducted a common garden experiment with plants from selfing and outcrossing populations as well as their between-population hybrids. Specifically, we asked whether there was isolation between outcrossing and selfing plants and their between-population hybrids through differences in (1) the timing or intensity of flowering; and/or (2) pollinator visitation. We found that phenology largely overlapped between plants from outcrossing and selfing populations. There were also no differences in pollinator preference related to mating system. Additionally, pollinators preferred to visit flowers on the same plant rather than exploring nearby plants, creating a large opportunity for self-fertilization. Overall, this suggests that pre-zygotic pre-pollination mechanisms do not strongly reproductively isolate plants from selfing and outcrossing populations of Arabidopsis lyrata .

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Otolith morphology and hearing abilities in cave- and surface-dwelling ecotypes of the Atlantic molly, Poecilia mexicana (Teleostei: Poeciliidae)

Hearing Research ◽

10.1016/j.heares.2010.04.001 ◽

2010 ◽

Vol 267 (1-2) ◽

pp. 137-148 ◽

Cited By ~ 23

Author(s):

Tanja Schulz-Mirbach ◽

Friedrich Ladich ◽

Rüdiger Riesch ◽

Martin Plath

Keyword(s):

Poecilia Mexicana ◽

Otolith Morphology ◽

Surface Dwelling ◽

Hearing Abilities

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Divergent Evolution of Male Aggressive Behaviour: Another Reproductive Isolation Barrier in Extremophile Poeciliid Fishes?

International Journal of Evolutionary Biology ◽

10.1155/2012/148745 ◽

2012 ◽

Vol 2012 ◽

pp. 1-14 ◽

Cited By ~ 24

Author(s):

David Bierbach ◽

Moritz Klein ◽

Vanessa Sassmannshausen ◽

Ingo Schlupp ◽

Rüdiger Riesch ◽

...

Keyword(s):

Sexual Selection ◽

Mate Choice ◽

Reproductive Isolation ◽

Hydrogen Sulphide ◽

Environmental Conditions ◽

Aggressive Behaviour ◽

Female Mate Choice ◽

Divergent Evolution ◽

Poecilia Mexicana ◽

Spring Area

Reproductive isolation among locally adapted populations may arise when immigrants from foreign habitats are selected against via natural or (inter-)sexual selection (female mate choice). We asked whether also intrasexual selection through male-male competition could promote reproductive isolation among populations of poeciliid fishes that are locally adapted to extreme environmental conditions [i.e., darkness in caves and/or toxic hydrogen sulphide (H2S)]. We found strongly reduced aggressiveness in extremophile Poecilia mexicana, and darkness was the best predictor for the evolutionary reduction of aggressiveness, especially when combined with presence of H2S. We demonstrate that reduced aggression directly translates into migrant males being inferior when paired with males from nonsulphidic surface habitats. By contrast, the phylogenetically old sulphur-endemic P. sulphuraria from another sulphide spring area showed no overall reduced aggressiveness, possibly indicating evolved mechanisms to better cope with H2S.

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It is lonely at the front: contrasting evolutionary trajectories in male and female invaders

Royal Society Open Science ◽

10.1098/rsos.160687 ◽

2016 ◽

Vol 3 (12) ◽

pp. 160687 ◽

Cited By ~ 27

Author(s):

Cameron M. Hudson ◽

Gregory P. Brown ◽

Richard Shine

Keyword(s):

Sexual Dimorphism ◽

Common Garden ◽

Limb Length ◽

Phenotypic Traits ◽

Evolutionary Changes ◽

Spatial Sorting ◽

Significant Heritability ◽

Selective Forces ◽

Major Shift ◽

Sex Disparity

Invasive species often exhibit rapid evolutionary changes, and can provide powerful insights into the selective forces shaping phenotypic traits that influence dispersal rates and/or sexual interactions. Invasions also may modify sexual dimorphism. We measured relative lengths of forelimbs and hindlimbs of more than 3000 field-caught adult cane toads ( Rhinella marina ) from 67 sites in Hawai'i and Australia (1–80 years post-colonization), along with 489 captive-bred individuals from multiple Australian sites raised in a ‘common garden’ (to examine heritability and reduce environmental influences on morphology). As cane toads spread from east to west across Australia, the ancestral condition (long limbs, especially in males) was modified. Limb length relative to body size was first reduced (perhaps owing to natural selection on locomotor ability), but then increased again (perhaps owing to spatial sorting) in the invasion vanguard. In contrast, the sex disparity in relative limb length has progressively decreased during the toads' Australian invasion. Offspring reared in a common environment exhibited similar geographical divergences in morphology as did wild-caught animals, suggesting a genetic basis to the changes. Limb dimensions showed significant heritability (2–17%), consistent with the possibility of an evolved response. Cane toad populations thus have undergone a major shift in sexual dimorphism in relative limb lengths during their brief (81 years) spread through tropical Australia.

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Experimental Evidence for Reproductive Isolation betweenAstrophytum coahuilense(H. Möller) Kayser andA. Capricornevar.Senile(Fric) Okumura (Cactaceae)

Haseltonia ◽

10.2985/026.020.0104 ◽

2015 ◽

Vol 20 ◽

pp. 13-21 ◽

Cited By ~ 3

Author(s):

Richard R. Montanucci

Keyword(s):

Reproductive Isolation ◽

Experimental Evidence

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Reduced opsin gene expression in a cave-dwelling fish

Biology Letters ◽

10.1098/rsbl.2009.0549 ◽

2009 ◽

Vol 6 (1) ◽

pp. 98-101 ◽

Cited By ~ 20

Author(s):

Michael Tobler ◽

Seth W. Coleman ◽

Brian D. Perkins ◽

Gil G. Rosenthal

Keyword(s):

Gene Expression ◽

Visual Function ◽

Opsin Gene ◽

Regressive Evolution ◽

Opsin Expression ◽

Poecilia Mexicana ◽

Evolutionary Step ◽

Surface Dwelling ◽

Blind Cave ◽

Intense Research

Regressive evolution of structures associated with vision in cave-dwelling organisms is the focus of intense research. Most work has focused on differences between extreme visual phenotypes: sighted, surface animals and their completely blind, cave-dwelling counterparts. We suggest that troglodytic systems, comprising multiple populations that vary along a gradient of visual function, may prove critical in understanding the mechanisms underlying initial regression in visual pathways. Gene expression assays of natural and laboratory-reared populations of the Atlantic molly ( Poecilia mexicana ) revealed reduced opsin expression in cave-dwelling populations compared with surface-dwelling conspecifics. Our results suggest that the reduction in opsin expression in cave-dwelling populations is not phenotypically plastic but reflects a hardwired system not rescued by exposure to light during retinal ontogeny. Changes in opsin gene expression may consequently represent a first evolutionary step in the regression of eyes in cave organisms.

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Limited phenological and pollinator-mediated isolation among selfing and outcrossing Arabidopsis lyrata populations

10.1101/2019.12.17.879361 ◽

2019 ◽

Author(s):

Courtney E. Gorman ◽

Lindsay Bond ◽

Mark van Kleunen ◽

Marcel E. Dorken ◽

Marc Stift

Keyword(s):

Reproductive Isolation ◽

Common Garden ◽

F1 Hybrids ◽

Common Garden Experiment ◽

Pollinator Visitation ◽

Arabidopsis Lyrata ◽

Pollinator Preference ◽

Pollination Mechanisms ◽

Self Fertilization ◽

Mechanistic Basis

AbstractTransitions from outcrossing to selfing have been a frequent evolutionary shift in plants and clearly play a role in species divergence. However, many questions remain about the initial mechanistic basis of reproductive isolation during the evolution of selfing. For instance, how important are prezygotic pre-pollination mechanisms (e.g. changes in phenology and pollinator visitation) in maintaining reproductive isolation between newly arisen selfing populations and their outcrossing ancestors? To test whether changes in phenology and pollinator visitation isolate selfing populations of Arabidopsis lyrata from outcrossing populations, we conducted a common garden experiment with plants from selfing and outcrossing populations as well as their F1 hybrids. Specifically, we asked whether there was isolation between outcrossing and selfing plants and their F1 hybrids through differences in 1) the timing or intensity of flowering; and/or 2) pollinator visitation. We found that phenology largely overlapped between plants from outcrossing and selfing populations. There were also no differences in pollinator preference related to mating system. Additionally, pollinators preferred to visit flowers on the same plant rather than exploring nearby plants, creating a large opportunity for self-fertilization. Overall, this suggests that prezygotic pre-pollination mechanisms do not strongly reproductively isolate plants from selfing and outcrossing populations of Arabidopsis lyrata.

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