Reproductive Capacity Evolves in Response to Ecology through Common Changes in Cell Number in Hawaiian Drosophila

Sarikaya, Didem P.; Church, Samuel H.; Lagomarsino, Laura P.; Magnacca, Karl N.; Montgomery, Steven L.; Price, Daniel O.; Kaneshiro, Kenneth Y.; Extavour, Cassandra G.

doi:10.1016/j.cub.2019.04.063

Cited by 21 publications

(54 citation statements)

References 58 publications

(119 reference statements)

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“…In this species, adult ovariole number is determined by cell proliferation and rearrangement during larval development [ 59 , 60 ]. Variation in adult number is derived primarily from variation in the number of ‘terminal filament precursor cells' [ 61 , 62 ], as well as from variation in the number of those precursor cells that group together to form the structure that initiates ovariole formation, known as a ‘terminal filament' [ 63 ]. Across species of Drosophila , variation in average adult ovariole number results primarily from variation in the average number of terminal filament precursor cells [ 62 ].…”

Section: Discussionmentioning

confidence: 99%

Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution

et al. 2021

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The number of offspring an organism can produce is a key component of its evolutionary fitness and life history. Here we perform a test of the hypothesized trade-off between the number and size of offspring using thousands of descriptions of the number of egg-producing compartments in the insect ovary (ovarioles), a common proxy for potential offspring number in insects. We find evidence of a negative relationship between egg size and ovariole number when accounting for adult body size. However, in contrast to prior claims, we note that this relationship is not generalizable across all insect clades, and we highlight several factors that may have contributed to this size-number trade-off being stated as a general rule in previous studies. We reconstruct the evolution of the arrangement of cells that contribute nutrients and patterning information during oogenesis (nurse cells), and show that the diversification of ovariole number and egg size have both been largely independent of their presence or position within the ovariole. Instead, we show that ovariole number evolution has been shaped by a series of transitions between variable and invariant states, with multiple independent lineages evolving to have almost no variation in ovariole number. We highlight the implications of these invariant lineages on our understanding of the specification of ovariole number during development, as well as the importance of considering developmental processes in theories of life-history evolution.

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Section: Discussionmentioning

confidence: 99%

Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution

et al. 2021

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“…In this species, the number of ovarioles can vary between the left and right ovaries within an individual, as well as across individuals within a population 57,58 . This variation is derived primarily from variation in the number of "terminal filament precursor cells" 59,60 , as well as from variation in the number of those precursor cells that group together to form the structure that initiates ovariole formation, known as a "terminal filament" 61 . Across species of Drosophila, variation in average adult ovariole number results primarily from variation in the average number of terminal filament precursor cells 60 .…”

Section: Discussionmentioning

confidence: 99%

Repeated loss of variation in insect ovary morphology highlights the role of developmental constraint in life-history evolution

Church

Medeiros

Donoughe

et al. 2020

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AbstractThe number of offspring an organism can produce is a key component of its evolutionary fitness and lifehistory. Here we perform a test of the hypothesized trade off between the number and size of offspring using thousands of descriptions of the number of egg-producing compartments in the insect ovary (ovarioles), a common proxy for potential offspring number in insects. In contrast to prior claims, we find that ovariole number is not generally negatively correlated with the size of insect eggs, and we highlight several factors that may have contributed to this size-number trade off being strongly asserted in previous studies. We reconstruct the evolutionary history of the nurse cell arrangement within the ovariole, and show that the diversification of ovariole number and egg size have both been largely independent of nurse cell presence or position within the ovariole. Instead we show that ovariole number evolution has been shaped by a series of transitions between variable and invariant states, with multiple independent lineages evolving to have almost no variation in ovariole number. We highlight the implications of these invariant lineages on our understanding of the specification of ovariole number during development, as well as the importance of considering developmental processes in theories of life-history evolution.

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“…For morphological data on wing, body, and thorax length, we digitized data from 26 publications 24,25,27,37,38,[42][43][44]66,[68][69][70][71][72][73][74][75][76][77][78][79][80][81][82][83][84] .…”

Section: Estimating Ecological and Morphological Evolutionary Transitionsmentioning

confidence: 99%

“…In 2008, Magnacca and colleagues reviewed host plant and substrate records and found that, while many species can be considered specialists to species or substrate, host shifting was common and many species occasionally use non-preferred substrates 39 . The type of oviposition substrate has been suggested as a driver for diversification of the reproductive traits ovariole number and egg size 15,37,38 . However, the previous reconstruction of oviposition substrate by Kambysellis and colleagues (1997) 15 was performed with a phylogeny that included only three non-PNA species, and was therefore unable to resolve the ancestral oviposition substrate for Hawaiian Drosophila or to identify when evolutionary shifts in substrate outside of PNA were likely to have occurred.…”

Section: Ancestral State Reconstruction Of Oviposition and Larval Feeding Ecologymentioning

confidence: 99%

“…Resolving these relationships is critical for our understanding of the morphological and ecological evolution of these flies [14][15][16] . Hawaiian Drosophila demonstrate a large diversity in body size 34 , wing size 35 , and egg size 36 ; in the number and position of structural features such as wing spots 35 ; in the number of egg-producing units in the ovary (ovarioles) 37,38 ; and in the type of substrate used for oviposition and larval feeding 15,39 . Some clades demonstrate unique suites of morphological and behavioral traits, whose evolutionary history is unclear because of uncertainties in the phylogeny.…”

Section: Introductionmentioning

confidence: 99%

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Phylotranscriptomics reveals discordance in the phylogeny of Hawaiian Drosophila and Scaptomyza (Diptera: Drosophilidae)

Church

Extavour

2021

Preprint

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Island radiations present natural laboratories for studying the evolutionary process. The Hawaiian Drosophil-idae are one such radiation, with nearly 600 described species and substantial morphological and ecological diversification. These species are largely divided into a few major clades, but the relationship between these clades remains uncertain. Here we present 12 new assembled transcriptomes from across these clades, and use these transcriptomes to resolve the base of the evolutionary radiation. We recover a new hypothesis for the relationship between clades, and demonstrate its support over previously published hypotheses. We then use the evolutionary radiation to explore dynamics of concordance in phylogenetic support, by analyzing the gene and site concordance factors for every possible topological combination of major groups. We show that high bootstrap values mask low evolutionary concordance, and we demonstrate that the most likely topology is distinct from the topology with the highest support across gene trees and from the topology with highest support across sites. We then combine all previously published genetic data for the group to estimate a time-calibrated tree for over 300 species of drosophilids. Finally, we digitize dozens of published Hawaiian Drosophilidae descriptions, and use this to pinpoint probable evolutionary shifts in reproductive ecology as well as body, wing, and egg size. We show that by examining the entire landscape of tree and trait space, we can gain a more complete understanding of how evolutionary dynamics play out across an island radiation.

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Reproductive Capacity Evolves in Response to Ecology through Common Changes in Cell Number in Hawaiian Drosophila

Cited by 21 publications

References 58 publications

Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution

Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution

Repeated loss of variation in insect ovary morphology highlights the role of developmental constraint in life-history evolution

Phylotranscriptomics reveals discordance in the phylogeny of Hawaiian Drosophila and Scaptomyza (Diptera: Drosophilidae)

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