<i>Cladocroce caelum</i> (Porifera) has a specialized growth region and a transcriptional regionalization across its body axis

Sponges (Porifera) are traditionally considered to lack defined body axes and regional specialization. Understanding whether sponges exhibit preferential growth regions and axial patterning is essential for elucidating the evolution of metazoan body plans. Here, we compared two body regions of the repent morph of <i>Cladocroce caelum</i> (Demospongiae): the proximal region, containing fully developed aquiferous system modules, and the distal region, hypothesized as the primary growth region. Our findings show that specimens predominantly grow from the distal region, where archaeocytes constitute the main cell type (mean 65.3%), whereas the proximal region features aquiferous system modules primarily composed of choanocytes (47%). To further explore molecular differences, we assembled a <i>de novo</i> reference transcriptome for <i>C. caelum</i>, recovering 99% of universal eukaryotic orthologous genes and 94% of metazoan orthologs. RNA-seq analysis revealed the expression of genes associated with the germline, stem cells, and developmental signaling pathways in both regions. However, we identified 11,421 differentially expressed genes (3,506 upregulated in the proximal region and 7,925 in the distal region). Notably, genes involved in the WNT, TGF-β, and MAPK pathways-key regulators of development and cell proliferation-were upregulated in the distal region. These findings provide morphological and molecular evidence of regional specialization in <i>C. caelum</i>, supporting the existence of a preferential growth region at the distal end. Our results suggest that despite the unique organization of the sponge body plan, some poriferans may possess specialized growth regions, akin to those in other metazoans.