Effects of maternal investment on larvae and juveniles of the annelidCapitella teletadetermined by experimental reduction of embryo energy content

Abstract

Experimental manipulations of the energy content of marine invertebrate embryos have been useful in testing key assumptions of life history theory, especially those concerning relationships between egg size, length of the planktonic period, and juvenile size and quality. However, methods for such “allometric engineering” experiments have been available for only a limited set of taxa (those with regulative early development, e.g., cnidarians and echinoderms). Here, we describe a method for the reduction of embryo energy content in the spirally cleaving embryos of a marine annelid, Capitella teleta, by targeted deletion of endodermal precursor cells. Embryos of C. teleta in which up to three cells (the macromeres 3A, 3B, and 3C) were deleted formed morphologically normal lecithotrophic larvae that were much smaller than larvae developing from control embryos. Experimental larvae metamorphosed at high rates, forming juveniles that were smaller than control juveniles. Juveniles derived from treated embryos had functional midguts, ingested and digested food, and grew into sexually mature adults. These results are consistent with those from previous allometric engineering studies of echinoid echinoderms, which suggest that in facultatively planktotrophic or lecithotrophic species, little maternally derived energy is used for construction of the larval body; instead, the majority is allocated to the formation of a large, high‐quality juvenile. Cleavage programs are highly conserved among divergent spiralian taxa (e.g., molluscs, nemerteans, and platyhelminths), so this method will likely be applicable to a diverse set of embryos. Similar experiments carried out in these diverse taxa will be extremely useful for evaluating inferences on relationships between egg size, length of the planktonic period, and juvenile size and quality previously based only on experiments on echinoid echinoderms.

A comparative analysis of egg provisioning using mass spectrometry during rapid life history evolution in sea urchins

“…However, in 6‐day old unfed juveniles (2 days postmetamorphosis), 70% of DAGE levels remain, followed by 49% remaining in 14‐day old juveniles (Byrne & Sewell, ). These results support the idea that elevated energy store deposition in lecithotrophic marine invertebrates may be more important for the development of a high‐quality juvenile than for supporting embryogenesis and construction of the larval body form, as previously suggested for other sea urchins (Alcorn & Allen, ), sea stars (Moreno & Hoegh‐Guldberg, ), and polychaetes (Pernet, Amiel, & Seaver, ). Taken together, these findings highlight the importance of considering the linkage between temporally disparate life history phases when investigating the impacts and constraints of adaptations associated with life history evolution (Marshall & Morgan, ).…”

Variation in spiralian development: insights from polychaetes

“…The strongest indication that polychaetes have organizing activity came from experiments in which the first cleavage was equalized, resulting in the formation of double embryos in Chaetopterus and Nereis (Henry andMartindale, 1987, Tyler, 1930). Single cell laser deletions have proven to be a precise and reliable technique in Capitella (Pernet et al, 2012). In conjunction with a detailed knowledge of the fate map , laser deletions were successfully used to identify an organizing activity in Capitella (Amiel et al, 2013).…”

The gastropod foregut — evolution viewed through a developmental lens

“…A host of studies, mostly on various species of echinoderm larvae, have examined effects of experimental manipulation of egg or embryo size or direct changes to egg nutrient content (literature reviewed by Pernet et al 2012). These have generally found that "planktotrophs [use] most of their maternally provided energy to construct the larval body, and lecithotrophs [use] most of their maternally provided energy to provision the post-metamorphic body" (Pernet et al 2012, p.83).…”

“…Studies by Pernet and colleagues (Pernet and McHugh 2010;Pernet et al 2012;Jones et al 2016) have shown that cytoplasm is preferentially sequestered to macromeres during cleavage of annelid and gastropod embryos. A greater amount of cytoplasmic yolk in macromeres (which is typical of lecithotrophic larvae) is correlated with a slowdown in rate of development of midgut structures arising from these macromeres.…”