Early periods in Earth's history have seen a progressive increase in complexity of the ecosystems, but also dramatic crises decimating the biosphere. Such patterns are usually considered as large-scale changes among supra-specific groups, including morphological novelties, radiation, and extinctions. Nevertheless, in the same time, each species evolved by the way of micro-evolutionary processes, extended over millions of years into the evolution of lineages. How these two evolutionary scales interacted is a challenging issue because this requires bridging a gap between scales of observation and processes. The present study aims at transferring a typical macro-evolutionary approach, namely disparity analysis, to the study of fine-scale evolutionary variations in order to decipher what processes actually drove the dynamics of diversity at a micro-evolutionary level. The Late Frasnian to Late Famennian period was selected because it is punctuated by two major macro-evolutionary crises, as well as a progressive diversification of marine ecosystem. Disparity was estimated through this period on conodonts, tooth-like fossil remains of small eel-like predators that were part of the nektonic fauna. The study was focused on the emblematic genus of the period, Palmatolepis. Strikingly, both crises affected an already impoverished Palmatolepis disparity, increasing risks of random extinction. The major disparity signal rather emerged as a cycle of increase and decrease in disparity during the inter-crises period. The diversification shortly followed the first crisis and might correspond to an opportunistic occupation of empty ecological niche. The subsequent oriented shrinking in the morphospace occupation suggests that the ecological space available to Palmatolepis decreased through time, due to a combination of factors: deteriorating climate, expansion of competitors and predators. Disparity changes of Palmatolepis thus reflect changes in the structure of the ecological space itself, which was prone to evolve during this ancient period where modern ecosystems were progressively shaped.