Decoupled maternal and zygotic genetic effects shape the evolution of development

Abstract

Evolutionary transitions from indirect to direct development involve changes in both maternal and zygotic genetic factors, with distinctive population-genetic implications, but empirical data on the genetics of such transitions are lacking. The polychaete Streblospio benedicti provides an opportunity to dissect a major transition in developmental mode using forward genetics. Females in this species produce either small eggs that develop into planktonic larvae or large eggs that develop into benthic juveniles. We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. The likely fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.

The genome of the poecilogonous annelidStreblospio benedicti

“…There are 11 chromosome-level scaffolds, from 38-65 Mb in length. They correspond to the karyotype, which shows ten autosomes and one sex chromosome, and the 11 linkage groups constructed previously (Zakas et al 2018).…”

“…Chromonomer breaks superscaffolds in regions of low confidence (stretches of 'N' ambiguity) and rearranges them based on high-confidence markers in the genetic map. The S. benedicti genetic map was previously constructed from G2 families with 702 markers in 11 linkage groups (Zakas et al 2018). Chromonomer used 570 (81% of the total) informative markers to reconcile the reference to the genetic map.…”

No evidence for sibling or parent-offspring coadaptation in a wild population of blue tits, despite high power

“…However, the conditions under which parental effect and offspring alleles would be non-independent in order to generate the appropriate genetic correlations seem harder to fulfil. Although linkage disequilibrium may be strong enough to allow PO coadaptation if generated by population structure (Zakas et al 2018) or speciation (Capodeanu-Nägler et al 2018), within-population PO coadaptation would be harder to achieve. Indeed, Santure et al (2013) have shown that there is low linkage disequilibrium in the great tit, and assuming similar patterns hold in blue tits, the potential for such coadapted gene complexes to evolve in this species may be limited, and the lack of evidence for PO coadaptation unsurprising (Lande 1980;Hadfield 2012).…”

Unravelling spiral cleavage

“…CRISPR and transgenesis) and imaging approaches (Neal et al, 2019;Perry and Henry, 2015;Zantke et al, 2014;Gline et al, 2011;Song et al, 2002;Weisblat and Kuo, 2014) (Table 1). However, a broad range of other spiralian species have been or are being used to study spiral cleavage employing molecular approaches, includingbut not limited tothe annelids Owenia fusiformis and Streblospio benedicti (Zakas et al, 2018;Martín-Durán et al, 2018); the molluscs Tritia (also known as Ilyanassa) obsoleta, Biomphalaria glabrata, Patella vulgata, Lymnaea stagnalis, Antalis entalis and Acanthochitona crinita (Wanninger and Wollesen, 2018;Abe and Kuroda, 2019;Lambert and Nagy, 2001;Grande and Patel, 2009;Damen and Dictus, 1994); the nemerteans Cerebratulus lacteus, Lineus ruber and Micrura alaskensis (Martín-Durán et al, 2018;Hiebert and Maslakova, 2015;; the flatworm Prostheceraeus crozieri (Girstmair and Telford, 2019); and other spiralian species that have secondarily lost spiral cleavage, such as cephalopod molluscs (Tarazona et al, 2019), the bryozoan Membranipora membranacea (Vellutini et al, 2017), and the brachiopods Terebratalia transversa and Novocrania anomala (Martín-Durán et al, 2016). This combination of established and emerging research systems covering most major lineages of Spiralia is bringing a more comprehensive understanding of spiral cleavage, the plasticity and regularities of this mode of development, and the mechanisms that generate a vast diversity of morphological outcomes from a widely shared embryonic program.…”