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.
Highlights
Offspring number is a fundamental parameter in the study of life history [1]
Our results showed that when considering body size, the slope of the regression of egg size and ovariole number is more negative than we would expect to observe by chance, as assessed by comparing to data simulated with no evolutionary correlation
Egg size and ovariole number are often used as proxies for offspring fitness [50] 7 and number [44,45], respectively, and it has been predicted that insects with more ovarioles lay smaller eggs than insects with fewer ovarioles [5,6,21,42]
Summary
Offspring number is a fundamental parameter in the study of life history [1]. This number differs widely between organisms [1], and its variation is the foundation for several hypotheses about life-history evolution, including the prediction that there is an evolutionary trade-off between the number of offspring and their size (e.g. egg size) [1,2,3]. We combined these data with published datasets of egg size [9], fecundity [10,11] and body size [12], to test hypotheses about the evolutionary trade-off between offspring size and number In these analyses, we used an existing phylogeny of insects [13] to analyse evolutionary patterns in ovariole number, and found that hypotheses about life-history evolution do not hold generally true across insects. We used an existing phylogeny of insects [13] to analyse evolutionary patterns in ovariole number, and found that hypotheses about life-history evolution do not hold generally true across insects We combined these data with published observations of the mode of oogenesis [7], and reconstructed the evolutionary history of the presence and position of nurse cells that contribute to the oocyte during oogenesis. We propose that the developmental mechanisms used to establish ovariole number in well-studied insects such as Drosophila melanogaster are unlikely to regulate ovariole number in all insects
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