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

Abstract

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.

Maternal control over caste allocation in the ant Cardiocondyla obscurior

“…The female reproductive apparatus is conserved in insects, and consists of two ovaries, the oviduct, the uterus, accessory glands and the spermatheca. Large variation can be found in the number of ovarioles making up each ovary, ranging from 1 in a dung beetle, 15-20 in the fruit fly Drosophila melanogaster [19], ∼200 in honey bees [37] to more than 1000 in some termite and ant species [38]. Six ovarioles in C. obscurior and Cardiocondyla nuda queens [39] mark the lower end in ants, thus allowing detailed study of ovary development in a simple model.…”

Prey life‐history influences the evolution of egg mass and indirectly reproductive investment in a group of free‐living insect predators

“…We confirm this hypothesis. Our second hypothesis stated that coccidophagous species should have smaller reproductive investment, which was estimated by ovariole numbers (Church et al, 2021), compared to aphidophagous ladybirds because they have to allocate more resources to searching for prey. Contrary to aphids, coccids are more difficult to find because they are highly aggregated (Ioannou et al, 2011; Taylor, 1977).…”

“…Church et al (2021) show that ovariole number is a reliable proxy for life-time fecundity, which is an expression of reproductive investment. We use a generalized linear mixed-effects model (GLMM) with a Poisson distribution and with random intercepts and slopes to assess the relationshipsTA B L E 2 F I G U R E 1…”

Protective geometry and reproductive anatomy as candidate determinants of clutch size variation in pentatomid bugs

“…Using the ovariole number database of Church et al (2021) as a starting point, we conducted a literature search of ovariole numbers per ovary in the Pentatomidae. While ovariole number per ovary from most pentatomid species in the literature was seven, in agreement with all entries for pentatomids in the Church et al (2021) database, we found that at least two species in the tribe Strachinii only have six ovarioles per ovary (Benedek 1968, Grodowitz et al 2019).…”

“…Ovariole numbers have been hypothesized to be determinants of clutch sizes in pentatomids (Kiritani and Hokyo 1965; Panizzi and Herzog 1984; Matesco et al 2008; Matesco et al 2009) as well as total lifetime reproductive output in other insect lineages (e.g., Price 1974; Ware et al 2008; Sarikaya et al 2019; Church et al 2021). Church et al (2021) recently reported that several insect taxa, including the Pentatomidae, have evolved invariant, or near-invariant, ovariole numbers. How near-invariant ovariole numbers might influence clutch size variation is currently unclear.…”