Complex heterochrony underlies the evolution ofCaenorhabditis eleganshermaphrodite sex allocation

Abstract

Hermaphroditic organisms are key models in sex allocation research, yet the developmental processes by which hermaphrodite sex allocation can evolve remain largely unknown. Here we use experimental evolution of hermaphrodite-male (androdioecious) Caenorhabditis elegans populations to quantify the developmental changes underlying adaptive shifts in hermaphrodite sex allocation. We show that the experimental evolution of increased early-life self-fertility occurred through modification of a suite of developmental traits: increased self-sperm production, accelerated oogenesis and ovulation, and increased embryo retention. The experimental evolution of increased self-sperm production delayed entry into oogenesis-as expected, given the sequentially coupled production of self-spermatogenesis and oogenesis. Surprisingly, however, delayed oogenesis onset did not delay reproductive maturity, nor did it trade-off with gamete or embryo size. Comparing developmental time dynamics of germline and soma indicates that the evolution of increased sperm production did not delay reproductive maturity due to a globally accelerated larval development during the period of self-spermatogenesis. Overall, heterochrony in gametogenesis and soma can explain adaptive shifts in hermaphrodite sex allocation.

Shorter life and reduced fecundity can increase colony fitness in virtual Caenorhabditis elegans

“…It does this not only by consumer sacrifice‐type adaptive death, as we initially proposed, but also through a reproductive schedule that generates an optimal population structure (Figure 6d). This joins a growing list of strategies by which androdioecious Caenorhabditis maximize early reproduction and population growth, including an early switch from sperm to egg production (Hodgkin & Barnes, 1991; Poullet et al, 2016), reduction of male frequency by various mechanisms (Garcia, LeBoeuf, & Koo, 2007; LaMunyon & Ward, 1997; Stewart & Phillips, 2002; Yin & Haag, 2019) and even earlier onset of reproduction in adults born from the first eggs (Perez, Francesconi, Hidalgo‐Carcedo, & Lehner, 2017). Plausibly, reduction of individual fitness to minimize futile food consumption can only increase fitness in organisms such as C. elegans (colonial and with a dispersal form).…”

Convergent evolution of sperm gigantism and the developmental origins of sperm size variability inCaenorhabditisnematodes

“…Females were then washed twice in M9 buffer and mounted in DAPI-containing Vectashield medium (Vector Laboratories, Inc., Burlingame, CA, USA). Imaging and sperm counts were performed as previously described (Poullet et al 2015(Poullet et al , 2016. In brief, images were taken at 40× magnification as Z-stacks covering the entire thickness of the animal using an epifluorescence microscope.…”

“…In general, nematode spermatozoa usually lack cilia or flagella (Lee 2002), unlike the sperm cells of insects and mammals, so that changes in sperm size must be coupled to cell volume. In the androdioecious nematode C. elegans multiple lines of evidence implicate cell size as a key component of sperm competitive ability: (i) males make larger sperm than hermaphrodites, with male sperm consistently outcompeting hermaphrodite sperm (Ward and Carrel 1979;LaMunyon and Ward 1995), (ii) larger C. elegans male sperm are competitively superior and crawl faster (LaMunyon and Ward 1998), and (iii) experimentally enhanced male-male competition leads to the evolution of larger sperm (LaMunyon and Ward 2002;Palopoli et al 2015;Poullet et al 2016). C. elegans males (and hermaphrodites) have small sperm compared to related obligatorily outcrossing species (LaMunyon and Ward 1999;Baldi et al 2011), which is thought to reflect part of a "selfing syndrome" in species like C. elegans that reproduce primarily by self-fertilization and so experience reduced sperm competition in nature (LaMunyon and Ward 1999;Cutter 2015).…”

Pheromone modulates two phenotypically plastic traits – adult reproduction and larval diapause – in the nematode Caenorhabditis elegans

“…This is compatible with our results, where early reproduction was successfully selected for, though in this case in a pheromone-dependent manner. Other work selecting for early reproduction has shown now many sub-components of reproduction (such as production of hermaphrodite sperm, oogenesis and ovulation rate, and embryo retention times) are malleable traits which respond to selection [ 27 ].…”